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. 2019 Mar 6;56(1):66–74. doi: 10.2478/helm-2018-0035

Helminths of Mustelids with Overlapping Ecological Niches: Eurasian Otter Lutra Lutra (Linnaeus, 1758), American Mink Neovison Vison Schreber, 1777, and European Polecat Mustela Putorius Linnaeus, 1758

D Nugaraitė 1,*, V Mažeika 1,*, A Paulauskas 1,*
PMCID: PMC6662030  PMID: 31662675

Summary

This study presents the helminthological data on three mustelid species with overlapping ecological niches in Lithuania. In general, 14 helminth species or higher taxa were reported from all mustelids: Isthmiophora melis, Strigea strigis metacercariae, Pseudamphistomum truncatum, Alaria alata mesocercariae, Phyllodistomum folium, Opisthorchis felineus, Metametorchis skrjabini, Mesocestoides sp., Taenia martis, Aonchotheca putorii, Crenosoma schachmatovae, Eucoleus aerophilus, Molineus patens, and Nematoda g. sp. The largest number of helminths was detected in M. putorius (11) and N. vison (10) from wetlands; 7 helminths were detected in M. putorius from forests, and 8 in N. vison and 4 in L. lutra from water bodies. Habitat-related differences were found in the abundance and prevalence of E. aerophilus in M. putorius. M. putorius has higher indices of infection by I. melis, S. strigis metacercariae, and E. aerophilus compared to N. vison in wetlands. Differences in the abundance and prevalence of P. truncatum among N. vison and L. lutra in water bodies have been observed. Helminths detected in N. vison in the present study are native European parasites.

Keywords: Lutra lutra, Neovison vison, Mustela putorius, helminths

Introduction

The Eurasian otter Lutra lutra (Linnaeus, 1758) (subfamily Lutrinae), the American mink Neovison vison Schreber, 1777 and the European polecat Mustela putorius Linnaeus, 1758 (subfamily Mustelinae) are mammals belonging to the family Mustelidae, with different affinity to the aquatic environment.

It is thought, that L. lutra originated in Asia and spread into Europe at the latest Pleistocene and early Holocene (Willemsen, 1992). Due to the loss of the riparian habitat, water pollution, polychlorinated biphenyls (PCBs) concentrations, hunting, declining food resources and road traffic accidents, L. lutra population declined in all of its distribution during the 20th century (MacDonald and Mason, 1988; Lodé, 1993b; Roos et al., 2015). Today L. lutra is listed as “Near Threatened” though it has one of the widest distributions of all Palearctic mammals (cover Europe, Asia and North Africa) (Roos et al., 2015). L. lutra is semi-aquatic mustelid found in a variety of aquatic habitats (Mason and MacDonald, 1986), whose diet consists mainly of aquatic prey (Bonesi et al., 2004). The species has been the subject of several more detailed helminthological studies, mainly in Belarus (Shimalov et al., 2000; Anisimova, 2002), Poland (Górski et al., 2010), Ukraine (Korol et al., 2016), United Kingdom (Fahmy, 1954; Jefferies et al., 1990; Weber, 1991; McCarthy and Hassett, 1993; Sherrard-Smith et al., 2015b), Germany (Schuster et al., 1988), and southwest Europe (Torres et al., 2004). Parasites act as a factor which could have an impact on the otter population dynamics, therefore the knowledge of the parasites may be useful for protecting the species.

N. vison was introduced to Europe at the beginning of 20th century from North America for the purpose of fur farming (Brzeziński and Marzec, 2003). As a result of escapes, deliberate releases, and farm damages by 1990s the feral N. vison population was registered almost in all European countries (Bonesi and Palazon, 2007; Lecis et al., 2008). Due to competition for food resources and space, N. vison is considered as an invasive species which could have an impact on the decline or disappearance of the European mink Mustela lutreola (Linnaeus, 1761) population in Europe (Maran and Henttonen, 1995). More recently N. vison has been considered as having a negative impact on the populations of L. lutra and M. putorius (MacDonald and Harrington, 2003; Melero et al., 2012). N. vison as well as L. lutra are semi-aquatic mustelids, however N. vison exploits both aquatic and terrestrial prey (Bonesi et al., 2004). The study of parasites related to the N. vison invasion in new regions is important due to possibility of introduction of new parasites to endemic host and transfer of endemic parasites to a new host. The impact of the introduced N. vison on parasite transmission has been studied (e.g., Ivanov and Semenova, 2000; Sherrard-Smith et al., 2015a; Martínez-Rondán et al., 2017).

M. putorius occurs throughout the Western Palearctic (Mitchell-Jones et al., 1999). In the last century its population sharply declined across Europe due to increase in human activities (Baghli et al., 2005). Today the species is listed as Least Concern in the IUCN Red List of Threatened Species (Skumatov et al., 2016). In northern and central Europe M. putorius is known to occupy a variety of habitat types: rivers, marshes, forests, woodland, farms, and villages (Jędrzejewski et al., 1993; Lodé, 1994; Baghli et al., 2005). According to Rondinini et al. (2006) the species is strongly associated with riparian areas in mainland Europe. Based on that, all three mustelid species (L. lutra, N. vison, and M. putorius) could present competition among them, because they exhibit overlap in diet and habitat preference (Lodé, 1993b; Bonesi et al., 2004).

No studies of L. lutra helminths from Lithuania have been reported to date. There is also poor documentation of N. vison and M. putorius parasites in this country. Earlier, unidentified nematodes and Isthmiophora melis (Schrank, 1788) Lühe, 1909 were reported in M. putorius (Maldžiūnaitė, 1959; Kazlauskas and Prūsaitė, 1976). Larvae of Trichinella Railliet, 1895 and Alaria alata (Goeze, 1782) were also documented in this host species (Grikienienė et al., 2001; Senutaitė and Grikienienė, 2001). Helminths of mustelids, including N. vison and M. putorius were reported by Nugaraitė et al. (2014).

The aim of this study was to explore the helminth communities of three mustelids with overlapping ecological niches: L. lutra, N. vison, and M. putorius.

Material and Methods

Carcasses of 6 L. lutra, 59 N. vison, and 27 M. putorius were collected in different localities of Lithuania between 2013 and 2017 (Fig. 1). N. vison and M. putorius were hunted by hunters and collected from car accidents, while L. lutra individuals were collected only from car accidents. Mustelids were assigned to the closest habitat and grouped as follows: (1) forests – M. putorius (n = 18); (2) wetlands – N. vison (n = 39) and M. putorius (n = 8); and (3) water bodies (rivers, lakes, and lagoons) – N. vison (n = 20) and L. lutra (n = 6). All carcasses were stored at -20°C until examination. Mustelids were examined using the method of total helminthological dissection of individual organs (Ivashkin et al., 1971). Frontal sinuses, connective tissue between the muscle fibres, trachea, lungs, heart, liver, gall bladder, kidney, urinary bladder, and entire gastrointestinal tract (stomach, small and large intestines) were analysed. Parasites were collected and stored in 70 % ethanol until studied.

Fig. 1.

Fig. 1

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Collection sites of Lutra lutra (LL), Neovison vison (NV), and Mustela putorius (MP) in Lithuania. (• – water bodies; ▴ – forests; ♦ – wetlands). The numbers on the map indicate the numbers of collected animals.

Temporary preparations were used for nematode morphological identification, while trematodes and cestodes were identified using permanent preparations. The identification was based on publications of Kozlov (1977), Sidorovich (1997), Kostadinova and Gibson (2002), Vieira et al. (2012), and Kontrimavičius (1969).

Helminthological terms were used according to the recommendations of Bush et al. (1997). The 95 % confidence intervals for prevalence were calculated as described by Rojtman and Lobanov (1985). Differences in the abundance and prevalence were tested using the Mann-Whitney U test and the Fisher’s exact test respectively.

Ethical Approval and/or Informed Consent

The research related to animals use has been complied with all the relevant national regulations and institutional policies for the care and use of animals. The study protocol no.

2017.03.22 No. 13. was approved by License of Environmental Protection Agency (EPA).

Results

Fourteen species or higher taxa of helminths were found in three species of mustelids from all habitats, i.e., 10 helminths in N. vison, 12 in M. putorius, and 4 in L. lutra (Table 1). The largest number of helminths was detected in M. putorius (11) and N. vison

Table 1.

Helminths of Lutra lutra, Neovison vison, and Mustela putorius from different habitats in Lithuania. A – mean abundance, SD – standard deviation, P, % – prevalence (95 % confidence intervals)

Lutra lutra Neovison vison Mustela putorius
Habitat A ± SD P, % A ± SD P, % A ± SD P, %
Trematoda
F 258.7 ± 400.7 77.7 (55.9 – 93.6)
Isthmiophora melis Wa 4.5 ± 2.8 50.0 (14.1 – 85.9) 34.3 ± 49.9 70.0 (48.2 – 87.9)
We 46.4 ± 60.1 77.0 (62.3 – 88.8) 449.5 ± 656.5 87.5 (57.0 – 100.0)
Strigea strigis F 24.6 ± 30.2 61.1 (37.8 – 82.0)
Wa 5.7 ± 11.5 30.0 (12.1 – 51.8)
metacercariae We 6.1 ± 14.9 28.2 (15.1 – 43.5) 13.3 ± 15.0 75.0 (40.9 – 97.1)
F 1.0 ± 3.9 16.6 (3.4 – 37.2)
Pseudamphistomum truncatum Wa 8.3 ± 11.6 66.7 (27.8 – 95.4) 0.3 ± 1.1 30.0 (12.1 – 51.8)
We 1.9 ± 5.4 17.9 (7.5 – 31.7) 0.3 ± 1.0 12.5 (0.0 – 43.0)
Alaria alata We - 7.6 (1.5 – 18.2) - 12.5 (0.0 – 43.0)
mesocercariae
Phyllodistomum folium* Wa 3.3 ± 8.2 16.7 (0.0 – 53.5)
Opisthorchis felineus We 0.1 ± 0.3 12.5 (0.0 – 43.0)
Metametorchis skrjabini We 1.1 ± 3.1 12.5 (0.0 – 43.0)
Cestoda
Wa 0.05 ± 0.2 5.0 (0.0 – 18.9)
Mesocestoides sp. We 0.07 ± 0.2 7.6 (1.5 – 18.2) 0.1 ± 0.3 12.5 (0.0 – 43.0)
Taenia martis We 0.02 ± 0.1 2.5 (0.0 – 10.0) 0.1 ± 0.3 12.5 (0.0 – 43.0)
Nematoda
F 32.5 ± 100.7 44.4 (22.5 – 67.6)
Aonchotheca putorii Wa 22.1 ± 48.0 50.0 (33.0 – 76.0)
We 10.6 ± 27.7 33.3 (19.3 – 49.0) 31.7 ± 43.4 50.0 (17.5 – 82.5)
Crenosoma F Wa 0.8 ± 2.7 15.0 (3.0 – 33.9) 3.2 ± 13.4 16.6 (3.4 – 37.2)
schachmatovae We 0.3 ± 1.0 10.2 (2.7 – 21.8) 1.7 ± 4.5 25.0 (2.9 – 59.1)
F 0.05 ± 0.2 5.5 (0.0 – 20.8)
Eucoleus aerophilus Wa 3.1 ± 13.1 10.0 (1.0 – 26.9)
We 1.4 ± 4.3 15.3 (5.8 – 28.5) 2.5 ± 3.9 62.5 (28.1 – 91.0)
F 2.8 ± 8.6 22.2 (6.4 – 44.1)
Molineus patens Wa 2.0 ± 7.7 20.0 (5.7 – 40.2)
We 0.7 ± 3.1 12.8 (4.2 – 25.2)
Nematoda g sp. Wa 1.6 ± 4.1 16.7 (0.0 – 53.5)
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Forests (F) – M. putorius (n = 18); Wetlands (We) – N. vison (n = 39); M. putorius (n = 8); Water bodies (Wa) – N. vison (n = 20); L. lutra (n = 6); *: Fish-specific trematode

(10) from wetlands; 7 helminths were detected in M. putorius from forests, 8 in N. vison and 4 in L. lutra from water bodies. N. vison and M. putorius from wetlands shared 9 helminths; M. putorius from forests and wetland shared 6 helminths.

The abundance and prevalence of Eucoleus aerophilus (Creplin, 1839) in M. putorius from wetlands was higher than in M. putorius from forests (p = 0.003/0.004 respectively). The abundance and prevalence of Strigea strigis (Schrank, 1788) metacercariae (p = 0.014/0.019) and E. aerophilus (p = 0.030/0.011) in M. putorius was higher (p<0.05) that in N. vison from wetlands. The abundance of I. melis in M. putorius was also higher that in N. vison (p = 0.010) from wetlands. N. vison from different habitats shared 8 helminth species, but differences in the abundance and prevalence of all helminth species were insignificant at p>0.05.

The abundance and prevalence of Pseudamphistomum truncatum (Rudolphi, 1819) in L. lutra from water bodies was higher that in N. vison (p = 0.000/0.002). A. alata mesocercariae was detected only in mustelids collected from wetlands. All three mustelids shared I. melis and P. truncatum.

Discussion

Of 14 helminths found and discussed in the present study, most are reported in at least one of three species of mustelids in other countries (Table 2), with the exception of Phyllodistomum folium (Olfers, 1816) and Crenosoma schachmatovae Kontrimavičius, 1969.

Table 2.

Helminth species of the present study reported in Lutra luira (LL), Neovison vison (NV), and Mustela putorius (MP) in other countries.

Helminths Host Country / Source
LL Germany (Schuster et al., 1988), Belarus (Sidorovich and Anisimova, 1999; Shimalov et al., 2000)
NV Germany (Zschille et al., 2004); France (Torres et al, 2008); Belarus (Shimalov and Shimalov, 2001); Caucasus (Itin and Kravchenko, 2016)
/. melis MP Germany (Kontrimavičius, 1969); Bulgaria (Kostedinova and Gibson, 2002), Hungary (Sugár and Matskási, 1978), Poland (Sołtys, 1962; Malczewski, 1964; Kontrimavičius, 1969); Belarus (Shimalov and Shimalov, 2002); Russia (Morozov et al., 1939; Kontrimavičius, 1969); Lithuania (Maldžiūnaitė, 1959; Kazlauskas and Prūsaitė, 1976); Former Czechoslovakia (Kontrimavičius, 1969; Mituch, 1972)
S. metacercariae strigis MP Belarus (Shimalov and Shimalov, 2002)
LL United Kingdom (Simpson et al., 2005; Sherrard-Smith et al, 2015b, 2016); Poland (Hildebrand et al, 2011); Belarus (Sidorovich et al., 1997; Shimalov et al., 2000); Germany (Schuster et al., 1988); Ukraine (Korol et al., 2016); Denmark; France; Germany; Sweden (Sherrard-Smith et al., 2016); Ireland (Hawkins et al., 2010)
P. truncatum NV England and Wales (Sherrard-Smith et al., 2015a, 2016); Ireland (Hawkins et al, 2010); Denmark (Skov et al, 2008); Volga Delta (Ivanov and Semenova, 2000); Caucasus (Itin and Kravchenko, 2016); Belarus (Sidorovich and Anisimova, 1997; Shimalov and Shimalov, 2001)
MP Belarus (Anisimova, 2002; Shimalov and Shimalov, 2002); Russia (Morozov et al., 1939; Kontrimavičius, 1969)
LL Poland (Górski et al., 2010); Belarus (Sidorovich et al., 1997; Shimalov et al., 2000)
A. mesocercariae alata NV Germany (Zschille et al, 2004); Caucasus (Itin and Kravchenko, 2016); Belarus (Shimalov and Shimalov, 2001); Volga Delta (Ivanov and Semenova, 2000)
MP Germany, Italy (Kontrimavičius, 1969); Belarus (Shimalov and Shimalov, 2002); Russia (Kontrimavičius, 1969; Kruchkova et al., 2008); Lithuania (Grikienienė et al., 2001)
LL Germany (Schuster et al, 1988); Belarus (Shimalov et al., 2000)
O. felineus NV Belarus (Shimalov and Shimalov, 2001)
MP Belarus (Shimalov and Shimalov, 2002)
M. skrjabini MP Gorky Oblast, Russia (Morozov, 1939)
LL Belarus (Shimalov et al., 2000)
M. lineatus NV Germany (Zschille et al, 2004); Caucasus (Itin and Kravchenko, 2016)
MP Belarus (Anisimova, 2002; Shimalov and Shimalov, 2002); Former Czechoslovakia (Mituch, 1972)
LL Germany (Schuster et al., 1988)
T. martis NV Iberian Peninsula (Torres et al., 2006); Germany (Zschille et al, 2004)
MP Belarus (Shimalov and Shimalov, 2002); Germany (Kontrimavičius, 1969); Former Czechoslovakia (Mituch, 1972)
LL Poland (Górski et al, 2010); France, Spain, Portugal (Torres et al., 2004); Belarus (Sidorovich et al, 1997; Shimalov et al., 2000); Latvia (Vismanis and Ozolins, 1998)
A. putorii NV France (Torres et al., 2008), Iberian Peninsula (Torres et al., 2006); Caucasus (Itin and Kravchenko, 2016); Belarus (Shimalov and Shimalov, 2001); Spain (Martinez-Rondán et al., 2017)
MP Belarus (Anisimova, 2002; Shimalov and Shimalov, 2002); Russia (Morozov, 1939); Poland (Górski et al., 2006); Iberian Peninsula (Torres et al., 1996); France (Torres et al., 2008); Belgium (Bernard, 1969); Former Czechoslovakia (Mituch, 1972)
E. aerophilus MP Russia (Morozov, 1939; Kontrimavičius, 1969; Kruchkova et al., 2008); Belarus (Shimalov and Shimalov, 2002); France (Torres et al., 2008)
M. patens NV Germany (Zschille et al, 2004); Iberian Peninsula (Miquel et al, 1993-1994; Torres et al., 2006); France (Torres et al., 2008); Belarus (Shimalov and Shimalov, 2001); Spain (Martínez-Rondán et al., 2017)
MP Belarus (Shimalov and Shimalov, 2002); Russia (Morozov, 1939; Kontrimavičius, 1969); Iberian Peninsula (Torres et al., 1996); France (Durette-Desset&Pesson, 1987; Torres et al., 2008); Belgium (Bernard, 1969); Switzerland (Mermod et al., 1983)
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P. folium was collected from L. lutra stomach. P. folium is a characteristic parasite of the northern pike Esox lucius Linnaeus, 1758, yet it is found in other fish as well (Bykhovskaya-Pavlovskaya and Kulakova, 1987). The occurrence of P. folium in L. lutra results from feeding on definitive host-fishes of the fluke.

C. schachmatovae have been described in stoat (Mustela ermine Linnaeus, 1758) from Karelia, Russia (Kontrimavičius, 1969). In Lithuania, C. schachmatovae have been reported in N. vison, M. putorius, and stone marten (Martes foina (Erxleben, 1777)) (Nugaraitė et al., 2014).

Cestodes of the genus Mesocestoides were not determined to the species level due to the poor preservation status of the specimens, however most measurements coincided with those of Mesocestoides lineatus (Goeze, 1782). This tapeworm is documented in other countries in M. putorius, N. vison, and L. lutra (Table 2).

Habitat-related differences were found in the abundance and prevalence of E. aerophilus in M. putorius. E. aerophilus has both a direct (by ingestion of larvated eggs) and indirect (by ingestion of oligochaetes containing larvae) life cycle (Anderson, 2000). The diet of M. putorius has not been studied in Lithuania, however according to other authors M. putorius does not feed on earthworms (Hammershøj et al., 2004; Malecha and Antczak, 2013). Therefore, the direct life cycle is likely the main mechanism of transmission of E. aerophilus to the host. Conditions for the survival of eggs are better in wetlands, consequently, wetlands offer a better environment for the life cycle realization.

In wetlands M. putorius and N. vison shared 9 helminths and, compared to N. vison, M. putorius was more parasitized by I. melis, S. strigis metacercariae, and E. aerophilus. Sharing the dens between N. vison and M. putorius may increase the risk of infection with the same species of helminths. Both mustelids do not have specialized diets, are generalist predators and can easily exploit different food resources (Bartoszewicz and Zalewski, 2003; Malecha and Antczak, 2013). According to Lodé (1993a) in wetlands N. vison mainly preys on fish and birds, whereas M. putorius consumes more rodents and amphibians. Amphibians, as an important component of the diet of M. putorius, were also suggested by other authors (Jędrzejewski et al., 1993; Hammershøj et al., 2004). So, the difference in diet could be a reason why M. putorius were more parasitized with helminths in whose life cycle amphibians play a role (i.e., I. melis, A. alata, and S. strigis). Transmission of A.

alata and S. strigis usually occurs through amphibians (Kontrimavičius, 1969; Shultz and Gvozdev, 1972), while I. melis is transmitted through both amphibians and freshwater fishes (Dönges, 1964; Radev et al., 2009). Reptiles, birds and small mammals can serve as paratenic hosts for A. alata (Kontrimavičius, 1969). For these two species, mustelids are paratenic hosts (Kontrimavičius, 1969) and are likely infected when they eat second intermediate hosts or, for A. alata, second intermediate or paratenic hosts.

Differences in the abundance and prevalence of P. truncatum among N. vison and L. lutra in water bodies have been observed. The life cycle of P. truncatum include two intermediate hosts; the first intermediate host is freshwater Bithynia snails and second is the Cyprinidae fish species (Hawkins et al., 2010). Fish is the major prey category in the diet of L. lutra (biomass 75.28 %) in Europe (Krawczyk et al., 2016). Despite that the diets of L. lutra and N. vison overlap (Bonesi et al., 2004) and both mustelids feed on intermediate hosts of P. truncatum, L. lutra is likely to consume more fishes than N. vison.

M. putorius and N. vison from wetlands harboured the richest helminth communities compared with other habitats. Such differences may be related to the differences in the composition and abundance of intermediate hosts among different habitats and the conditions for surviving of free-living stages of parasites which are better in wet environment.

In the present study I. melis and P. truncatum were detected in all three mustelid species. Detection of I. melis and P. truncatum in all mustelids is closely associated with their living environment and diet. Introduced N. vison and native L. lutra are semiaquatic

mustelids which coexist in many riparian habitats. Moreover, some studies suggest M. putorius preference for the aquatic environment (Jędrzejewski et al., 1993; Zabala et al., 2005; Rondinini et al., 2006). Diets of these mustelid species overlap and include intermediate hosts of these two flukes. L. lutra diet consists mainly of aquatic prey, N. vison and M. putorius exploit both aquatic and terrestrial prey (Bonesi et al., 2004).

In general, the helminths community of M. putorius was richer (12 helminths) compared with N. vison (10 helminths), and L. lutra (4 helminths). The helminth fauna of L. lutra in Lithuania is probably richer, however results in the present study are derived from small number of animals examined. It is related with L. lutra protection status in Europe. Despite the fact that its population is widely distributed across Lithuania (covers 95 % of the territory) (Baltrūnaitė et al., 2009), hunting has been prohibited since 1975 (Mickevičius, 1993; Baranauskas et al., 1994).

The richer helminth fauna of M. putorius is probably related with a wide variety of habitats used by this species.

Introduction of N. vison in Lithuania occurred after World War II as the result of releases from fur farms in Kaliningrad Oblast, Russia and Lithuania and introduction of animals from Tatarstan (Russia) (Prūsaitė et al., 1988; Balčiauskas, 1996). The invasion of N. vison in new regions may have led to the introduction of new parasites and their transfer to endemic hosts. Helminths of N. vison in North America have been reported by numerous authors (e.g., Beaver, 1941; Zabiega, 1996; Foster et al., 2007). A checklist of helminths in N. vison from Montana was reported by Barber and Lockard (1973). Some helminth species (i.e., Metorchis albidus (Braun, 1893), Aonchotheca mustelorum (Cameron and Parnell, 1933) (syn. Capillaria mustelorum), and Baylisascaris devosi (Sprent, 1952) (syn. Ascaris devosi)) detected in N. vison from Belarus are supposed as species arrived with this animal from its native area, i.e. North America (Anisimova, 2004).

All helminths detected in N. vison in our study are native European parasites, which are also common parasites of a wide range of European mustelids and other mammals. All helminth species found in N. vison are also found in M. putorius. Helminthological studies in other European countries show similar results that N. vison is parasitized by native parasites, e.g. in Spain (Torres et al., 2006; Martínez-Rondán et al., 2017) and France (Torres et al., 2008). Invasive N. vison could lose their original parasites, because feral populations come from animals raised in fur farms, where parasite cycling is aggravated. Invasive species are likely to accumulate parasites in the environments inhabited by closely related species (Parker and Gilbert, 2007). In our case infection of invasive N. vison with native parasites can be facilitated by contacts with taxonomically closely related native mustelids (e.g. M. putorius, etc.) and parasites being widespread generalist with a wide host range. It is worth mentioning that the ranges of some parasite species found in our study include invasive and natural range of N. vison (i.e., Palearctic and Nearctic). Helminths found by us are known in N. vison from North America: I. melis (Beaver, 1941), A. putorii (Zabiega, 1996; Foster et al., 2007), and M. patens (Foster et al., 2007). From all above we can conclude that all three studied mustelids exchange helminths and have common species. Helminths community structure is influenced by habitat. Our results show that the epidemiological role of invasive N. vison is in the maintenance of the life cycles of native parasites.

Acknowledgments

This research was financed by the Research Council of Lithuania (grant No. LEK-14/2012).

Footnotes

Conflict of Interest

Authors state no conflict of interest.

References

  1. Anderson R.C. Nematode Parasites of Vertebrates, their Development and Transmission 2nd Edition. Wallingford, UK: CABI Publishing; 2000. p. 650. [DOI] [Google Scholar]
  2. Anisimova E.I.. Comparative analysis of the helminthocenoses of the otter Lutra lutra and polecat Mustela putorius in Belarus. Helminthologia. 2002;39(2):87–90. [Google Scholar]
  3. Anisimova E.I.. Study on the European mink Mustela lutreola helminthocenoses in connection with the American mink M vison expansion in Belarus. Story of the study and review of the results. Helminthologia. 2004;41(4):193–196. [Google Scholar]
  4. Baghli A., Walzberg C., Verhagen R.. Habitat use by the European polecat Mustela putorius at low density in a fragmented landscape. Wildlife Biol. 2005;11(4):331–339. doi: 10.2981/0909-6396(2005)11[331:HUBTEP]2.0.CO;2. [DOI] [Google Scholar]
  5. Balčiauskas L.. Lithuanian Mammal Fauna Review. Hystrix. 1996;8(1-2):9–15. doi: 10.4404/hystrix-8.1-2-4087. [DOI] [Google Scholar]
  6. Balčiauskas L., Ulevičius A., Juškaitis R.. Mammals of Lithuania: status and protection. Säugetierschutz. Zeitschrift für Theriophylaxe (Delligsen) 1997;27:4–8. [Google Scholar]
  7. Baltrūnaitė L., Balčiauskas L., Matulaitis R., Stirkė V.. Otter distribution in Lithuania in 2008 and changes in the last decade. Est. J. Ecol. 2009;58(2):94–102. doi: 10.3176/eco.2009.2.03. [DOI] [Google Scholar]
  8. Baranauskas K., Mickevičius E., Macdonald S.M., Mason C.F.. Otter distribution in Lithuania. Oryx. 1994;28(02):128–130. doi: 10.1017/S003060530002843X. [DOI] [Google Scholar]
  9. Barber D.L., Lockard L.L.. Some helminths from mink in southwestern Montana, with a checklist of their internal parasites. Great Basin nat. 1973;33(1):53–60. [Google Scholar]
  10. Bartoszewicz M., Zalewski A.. American mink, Mustela vison diet and predation on waterfowl in the Słońsk Reserve, western Poland. Folia Zool. 2003;52:225–238. [Google Scholar]
  11. Beaver P.C.. Studies on the life history of Euparyphium melis (Trematoda: Echinostomidae) J. Parasitol. 1941;27(1):35–44. doi: 10.2307/3272884. [DOI] [Google Scholar]
  12. Bernard J.. Observations sur les helminthes parasites de mammifères et d’oiseaux de la faune de Belgique. Archives de l’Institut Pasteur de Tunis. 1969;46:137–193. In French. [Google Scholar]
  13. Bonesi L., Chanin P., Macdonald D.W.. Competition between Eurasian otter Lutra lutra and American mink Mustela vison probed by niche shift. Oikos. 2004;106(1):19–26. doi: 10.1111/j.0030-1299.2004.12763.x. [DOI] [Google Scholar]
  14. Bonesi L., Palazon S.. The American mink in Europe: Status, impacts, and control. Biol Conserv. 2007;134(4):470–483. doi: 10.1016/j.biocon.2006.09.006. [DOI] [Google Scholar]
  15. Brzeziński M., Marzec M.. The origin, dispersal and distribution of the American mink Mustela vison in Poland. Acta Theriol. 2003;48(4):505–514. doi: 10.1007/BF03192496. [DOI] [Google Scholar]
  16. Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W.. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 1997;83(4):575–583. doi: 10.2307/3284227. [DOI] [PubMed] [Google Scholar]
  17. Bykhovskaya-pavlovskaya I., Kulakova A.P. Bauer O.N. Key to the parasites of freshwater fish fauna of the USSR. Leningrad USSR: Nauka Publishing Leningrad branch; 1987. Class Trematoda Rudolphi, 1808; pp. 77–198. Volume 3. Parasitic Metazoans (part two) In Russian. [Google Scholar]
  18. Durette-desset M., Pesson B.. Molineus patens (Dujardin, 1845) (Nematoda, Trichostrongyloidea) et autres espèces décrites sous ce nom [Molineus patens (Dujardin, 1845) (Nematoda, Trichostrongyloidea) and other species described under this name] Ann. Parasitol. Hum. Comp. 1987;62(4):326–344. doi: 10.1051/parasite/1987624326. In French. [DOI] [Google Scholar]
  19. Dönges J.. A local, facultative Echinostomatide (Trematoda) type human pathogen and infection course in humans. Z. Parasitenkd. 1964;25(1):3. (In German) [Google Scholar]
  20. Fahmy M.A.M.. On some helminth parasites of the otter, Lutra lutra. J Helminthol. 1954;28(3-4):189–204. doi: 10.1017/S0022149X00032867. [DOI] [PubMed] [Google Scholar]
  21. Foster G.W., Cunningham M.W., Kinsella J.M., Owen M.. Parasitic helminths of free-ranging mink Neovison vison mink) from southern Florida. J. Parasitol. 2007;93(4):945–946. doi: 10.1645/GE-1172R.1. [DOI] [PubMed] [Google Scholar]
  22. Górski P., Zalewski A., Kazimierczak K., Kotomski G.. Coproscopical investigations of the European otter Lutra lutra from Białowieża Primeval Forest. Wiad Parazytol. 2010;56(2):179–180. [PubMed] [Google Scholar]
  23. Grikienienė J., Malakauskas M., Mažeikytė R., Balčiauskas L., Senutaitė J.. Lietuvos laukinių žinduolių raumenų parazitai (Sarcocystis, Trichinella, Alaria) [Muscle parasites Sarcocystis Trichinella Alaria of wild mammals in Lithuania] Theriologia Lituanica. 2001;1:29–46. In Lithuanian. [Google Scholar]
  24. Hammershøj M., Thomsen E.A., Madsen A.B.. Diet of free-ranging American mink and European polecat in Denmark. Acta Theriol. 2004;49(3):337–347. doi: 10.1007/BF03192532. [DOI] [Google Scholar]
  25. Hawkins C.J., Caffrey J.M., Stuart P., Lawton C.. Biliary parasite Pseudamphistomum truncatum (Opistorchiidae) in American mink Mustela vison and Eurasian otter Lutra lutra in Ireland. Parasitol Res. 2010;107(4):993–997. doi: 10.1007/s00436-010-1951-6. [DOI] [PubMed] [Google Scholar]
  26. Hildebrand J., Popiołek M., Zaleśny G., Piróg A.. A record of Pseudamphistomum truncatum (Rudolphi, 1819) (Digenea, Opisthorchiidae) in the Eurasian otter Lutra lutra L.) from Poland. Wiad. Parazytol. 2011;57(3):151–154. [PubMed] [Google Scholar]
  27. Itin G.S., Kravchenko V.M. Proceedings of the scientific conference Theory and Practice of the struggle against Parasitic Diseases. Moscow, Russia: 2016. Specific structure of helminthocenoses of wild carnivorous mammals in the landscape-geographical zones of the North-West Caucasus; pp. 194–198. May 17-18, 2016. In Russian. [Google Scholar]
  28. Ivanov V.M., Semenova N.N.. Parasitological consequences of animal introduction. Russ J Ecol. 2000;31(4):281–283. doi: 10.1007/BF02764062. [DOI] [Google Scholar]
  29. Ivashkin V.M., Kontrimavičius V.N., Nazarova N.S. Methods of collection and study of terrestrial mammal helminthes. Moscow, Russia: Nauka; 1971. p. 124. In Russian. [Google Scholar]
  30. Jędrzejewski W., Jędrzejevska B., Brzezinski M.. Winter habitat selection and feeding habits of polecats Mustela putorius in the Białowieza National Park, Poland. Z. Säugetierkd. 1993;58(2):75–83. [Google Scholar]
  31. Jefferies D.J., Hanson H.M., Harris E.A.. The prevalence of Pseudoterranova decipiens (Nematoda) and Corynosoma strumosum (Acanthocephala) in otters Lutra lutra from coastal sites in Britain. J. Zool. 1990;221(2):316–321. doi: 10.1111/j.1469-7998.1990.tb04003.x. [DOI] [Google Scholar]
  32. Kazlauskas J., Prūsaitė J. Helminths of carnivores in Lithuania. Acta Parasitol. Lituan. 1976;12:33–40. In Russian. [Google Scholar]
  33. Kontrimavičius V.L. Helminths of mustelids and trends in their evolution. Moscow, Russia: Nauka; 1969. p. 432. In Russian. [Google Scholar]
  34. Korol E.N., Varodi E.I., Kornyushin V.V., Malega A.M.. Helminths of wild predatory mammals (Mammalia, Carnivore) of Ukraine. Trematodes. Vestn. Zool. 2016;50(4):301–308. doi: 10.1515/vzoo-2016-0037. [DOI] [Google Scholar]
  35. Kostadinova A., Gibson D.I.. Isthmiophora Lühe, 1909 and Euparyphium Dietz, 1909 (Digenea: Echinostomatidae) re-defined, with comments on their nominal species. Syst. Parasitol. 2002;52(3):205–217. doi: 10.1023/A:1015789703396. [DOI] [PubMed] [Google Scholar]
  36. Kozlov D.P. Key to Helminths of Carnivorous Mammals of the USSR. Moscow, Russia: Nauka; 1977. p. 276. In Russian. [Google Scholar]
  37. Krawczyk A.J., Bogdziewicz M., Majkowska K., Glazaczow A.. Diet composition of the Eurasian otter Lutra lutra in different freshwater habitats of temperate Europe: a review and meta-analysis. Mammal Rev. 2016;46:106–113. doi: 10.1111/mam.12054. [DOI] [Google Scholar]
  38. Kruchkova E.N., Abalikhin B.G., Egorov S.V., Safiullin R.T.. Parasitofauna of mustelids in the central Non-Black Earth region of Russia. Veterinarija. 2008;9:34–36. In Russian. [Google Scholar]
  39. Lecis R., Ferrando A., Ruiz-olmo J., Manas S., Domingoroura X.. Population genetic structure and distribution of introduced American mink Mustela vison in Spain, based on microsatellite variation. Conserv. Genet. 2008;9(5):1149–1161. doi: 10.1007/s10592-007-9428-6. [DOI] [Google Scholar]
  40. Lodé T.. Diet composition and habitat use of sympatric polecat and American mink in western France. Acta Theriol. 1993a;38(2):161–166. doi: 10.4098/AT.arch.93-14. [DOI] [Google Scholar]
  41. Lodé T.. The decline of otter Lutra lutra populations in the region of the Pays de Loire, western France. Biol. Conserv. 1993b;65(1):9–13. doi: 10.1016/0006-3207(93)90190-C. [DOI] [Google Scholar]
  42. Lodé T.. Environmental factors influencing habitat exploitation by the Polecat Mustela putorius in western France. J. Zool. 1994;234(1):75–88. doi: 10.1111/j.1469-7998.1994.tb06057.x. [DOI] [Google Scholar]
  43. Macdonald S.M., Mason C.F.. Observations on an otter population in decline. Acta Theriol. 1988;33(30):415–434. [Google Scholar]
  44. Macdonald D., Harrington L.. The American mink: The triumph and tragedy of adaptation out of context. N.Z. J. Zool. 2003;30(4):421–441. doi: 10.1080/03014223.2003.9518350. [DOI] [Google Scholar]
  45. Malczewski A.. Przyczynek do znajomosci helmintofauny Mustelidae w Polsce. Wiad. Parazytol. 1964;10:565–567. In Polish. [PubMed] [Google Scholar]
  46. Maldžiūnaitė S.. Some data on the parasites of mustelids in the Lithuanian S.S.R. Acta Parasitol. Lithuan. 1959;2:57–59. In Russian. [Google Scholar]
  47. Malecha A.W., Antczak M.. Diet of the European polecat Mustela putorius in an agricultural area in Poland. Folia Zool. 2013;62(1):48–53. doi: 10.25225/fozo.v62.i1.a7.2013. [DOI] [Google Scholar]
  48. Maran T., Henttonen H.. Why is the European mink Mustela lutreola disappearing? - A review of the process and hypotheses. Annls. Zool. Fennici. 1995;32(1):47–54. [Google Scholar]
  49. Martínez-Rondán F.J., Ruiz De Ybáñez M.R., Tizzani P., López-Beceiro A.M., Fidalgo L.E., Martínez-Carrasco C.. The American mink Neovison vison is a competent host for native European parasites. Vet. Parasitol. 2017;247:93–99. doi: 10.1016/j.vetpar.2017.10.004. [DOI] [PubMed] [Google Scholar]
  50. Mason C.F., Macdonald S.M. Otters: ecology and conservation. Cambridge, New York: Cambridge University Press; 1986. p. 236. [Google Scholar]
  51. Melero Y., Plaza M., Santulli G., Saavedra D., Gosàlbez J., Ruíz-Olmo J., Palazón S.. Evaluating the effect of American mink, an alien invasive species, on the abundance of a native community: is coexistence possible? Biodivers. Conserv. 2012;21(7):1795–1809. doi: 10.1007/s10531-012-0277-3. [DOI] [Google Scholar]
  52. Mermod C., Debrot S., Marchesi P., Weber J.-M.. Le putois Mustela putorius L.) en Suisse romande. Revue Suisse de Zoologie. 1983;90:847–856. doi: 10.5962/bhl.part.117747. (In French) MICKEVIČIUS, E. (1993): The otter in Lithuania. IUCN Otter Spec. Group Bull 8: 29 – 31. [DOI] [Google Scholar]
  53. Mitchell-jones A., Bogdanowicz W., Krystufek B., Reijnders P.J.H., Spitzenberger F., Stubbe C., Thissen J.B.M., Vohralík V., Zima J. The Atlas of European mammals. London, UK: Academic Press; 1999. p. 484. [Google Scholar]
  54. Mituch J.. Helmintofauna mäsožravcov na Slovensku a v ČSSR [Helminths of carnivores in Slovakia and Czechoslovakia] Folia Venatoria. 1972;10(11):161–171. In Slovak. [Google Scholar]
  55. Miquel J., Feliu C., Torres J., Casanova J.C.. Corología de las especies de nematodos parásitas de carnívoros silvestres en Cataluña (NE península ibérica) [Corology of the nematode parasites of wild carnivores in Catalonia (NE Iberian Peninsula)] Miscellania Zoologica. 1993–1994;17:49–57. In Spanish. [Google Scholar]
  56. Моrozov F.N.. The parasitic worms of fur-bearing animals of the family Mustelidae of Gorky Oblast. Gor’kov. Gosud. Pedigog. Inst. 1939;4:3–44. In Russian. [Google Scholar]
  57. Nugaraitė D., Mažeika V., Paulauskas A.. Helminths of mustelids (Mustelidae) in Lithuania. Biologija. 2014;60(3):117–125. doi: 10.6001/biologija.v60i3.2970. [DOI] [Google Scholar]
  58. Parker I.M., Gilbert G.S.. When there is no escape: the effects of natural enemies on native, invasive, and noninvasive plants. Ecology. 2007;88(5):1210–1224. doi: 10.1890/06-1377. [DOI] [PubMed] [Google Scholar]
  59. Prūsaitė J., Mažeikytė R., Pauža D., Paužienė N., Juškaitis R., Mickus A., Grušas A., Skeiveris R., Bluzma P., Bielova O., Baranauskas K., Mačionis A., Balčiauskas L., Janulaitis Z. Lietuvos fauna [Fauna of Lithuania] Vilnius, Lithuania, Mokslas: 1988. p. 294. [Google Scholar]
  60. Radev V., Kanev I., Khrusanov D., Fried B.. Reexamination of the life cycle of Isthmiophora melis (Trematoda: Echinostomatidae) on material from southeast Europe. Parazitologiia. 2009;43(6):445–453. In Russian. [PubMed] [Google Scholar]
  61. Rojtman V.A., Lobanov A.L. Sonin M.D. Research on Morphology, Taxonomy and Biology of Bird Helminths. Proceedings of Helminthology Laboratory. Volume XXXIII. Nauka; Moscow: 1985. Method of estimation of parasite hemipopulation abundance in host population; pp. 102–123. In Russian. [Google Scholar]
  62. Rondinini C., Ercoli V., Boitani L.. Habitat use and preference by polecats Mustela putorius L.) in a Mediterranean agricultural landscape. J. Zool. 2006;269(2):213–219. doi: 10.1111/j.1469-7998.2006.00073.x. [DOI] [Google Scholar]
  63. Roos A., Loy A., De silva P., Hajkova P., Zemanová B.. Lutra lutra. http//www.iucnredlist.org IUCN2015 2015 IUCN Red List of Threatened Species. 2015;24:2018. Retrieved July. [Google Scholar]
  64. Schuster R., Schierhorn K., Heidecke D., Stubbe M.. The parasite fauna of East Germany. 9. The helminth fauna of Lutra lutra. Angew. Parasitol. 1988;29(2):107–111. In German. [PubMed] [Google Scholar]
  65. Senutaitė J., Grikienienė J.. Prevalence of Trichinella in muscle of some domestic and wild mammals in Lithuania and their impact on organism. Acta Zool. Lit. 2001;11(4):395–404. doi: 10.1080/13921657.2001.10512477. [DOI] [Google Scholar]
  66. Sherrard-smith E., Chadwick E.A., Cable J.. The impact of introduced hosts on parasite transmission: opisthorchiid infections in American mink Neovison vison. Biol. Invasions. 2015a;17(1):115–122. doi: 10.1007/s10530-014-0709-y. [DOI] [Google Scholar]
  67. Sherrard-smith E., Perkins S.E., Chadwick E.A., Cable J.. Spatial and seasonal factors are key determinants in the aggregation of helminths in their definitive hosts: Pseudamphistomum truncatum in otters Lutra lutra. Int. J. Parasitol. 2015b;45(1):75–83. doi: 10.1016/j.ijpara.2014.09.004. [DOI] [PubMed] [Google Scholar]
  68. Sherrard-smith E., Stanton D.W., Cable J., Orozco-terwengel P., Simpson V.R., Elmeros M., Van dijk J., Simonnet F., Roos A., Lemarchand C., Poledník L., Heneberg P., Chadwick E.A.. Distribution and molecular phylogeny of biliary trematodes (Opisthorchiidae) infecting native Lutra lutra and alien Neovison vison across Europe. Parasitol. Int. 2016;65(2):163–170. doi: 10.1016/j.parint.2015.11.007. [DOI] [PubMed] [Google Scholar]
  69. Shimalov V.V., Shimalov V.T., Shimalov A.V.. Helminth fauna of otter Lutra lutra Linnaeus, 1758) in Belorussian Polesie. Parasitol. Res. 2000;86(6):528. doi: 10.1007/s004360050708. [DOI] [PubMed] [Google Scholar]
  70. Shimalov V.V., Shimalov V.T.. Helminth fauna of the American mink Mustela vision Schreber, 1777) from Belorussian Polesie. Parasitol. Res. 2001;87(10):886–887. doi: 10.1007/s004360100461. [DOI] [PubMed] [Google Scholar]
  71. Shimalov V.V., Shimalov V.T.. Helminth fauna of the European polecat Mustela putorius Linnaeus, 1758) in Belorussian Polesie. Parasitol. Res. 2002;88(3):259–260. doi: 10.1007/s00436-001-0521-3. [DOI] [PubMed] [Google Scholar]
  72. Shultz R.S., Gvozdev E.V. Basics of general helminthology. Moscow, Russia: Nauka; 1972. p. 515. [Google Scholar]
  73. Sidorovich V.E. Mustelids in Belarus. Evolutionary Ecology, Demography and Interspecific Relationships. Minsk, Russia: Zolotoy uley publisher; 1997. p. 289. [Google Scholar]
  74. Sidorovich V.E., Anisimova E.I.. Peculiarities of helminthocenosis in the American mink population inhabiting a severely polluted rivers ecosystem (the Svisloch river, Belarus) Helminthologia. 1997;34:45–52. [Google Scholar]
  75. Sidorovich V.E., Anisimova E.I., Shimalov V.T., Bychkova E.I., Lauzhel G.O. Sidorovich V.E. Mustelids in Belarus Evolutionary ecology, demography and interspecific relationships. Minsk, Russia: Zolotoy uley publisher; 1997. Comparative analysis of the semiaquatic mustelid helminthocenosis; p. 194 – 199. [Google Scholar]
  76. Sidorovich V., Anisimova E.I.E.. Comparative Analysis or the Helminthocenoses of the Native Semiaquatic Mustelids Lutra lutra Mustela lutreola in Connection with the Width of Food Spectra. IUCN Otter Spec. Group Bull. 1999;16(2):76–78. [Google Scholar]
  77. Simpson V.R., Gibbons L.M., Khalil L.F., Williams J.L.R.. Cholecystitis in otters Lutra lutra and mink Mustela vison caused by the fluke Pseudamphistomum truncatum. Vet. Rec. 2005;157(2):49–52. doi: 10.1136/vr.157.2.49. [DOI] [PubMed] [Google Scholar]
  78. Skov J., Kania P.W., Jørgensen T.R., Buchmann K.. Molecular and morphometric study of metacercariae and adults of Pseudamphistomum truncatum (Opisthorchiidae) from roach Rutilus rutilus and wild American mink Mustela vison. Vet. Parasitol. 2008;155(3-4):209–216. doi: 10.1016/j.vetpar.2008.05.011. [DOI] [PubMed] [Google Scholar]
  79. Skumatov D., Abramov A.V., Herrero J., Kitchener A., Maran T., Kranz A., Sándor A., Saveljev A., Savour-soubelet A., Guinot-ghestem M., Zuberogoitia I.. Mustela putorius. http//www.iucnredlist.org IUCN2016 2016 IUCN Red List of Threatened Species. 2016;16:2018. Retrieved July. [Google Scholar]
  80. Sołtys A.. Helminth parasites of Mustelidae of the Lublin Palatinate. Acta Parasitol. Polonica. 1962;10(1/11):73–76. [Google Scholar]
  81. Sugá R L., Matská Si I. Occurrence of Isthmiophora melis (Schrank, 1788) and Alaria alata (Goeze, 1782) in wild carnivora in Hungary. Parasitol. Hung. 1978;11:142–142. [Google Scholar]
  82. Torres J., Feliu C., Miquel J., Casanova J.C., García-Perea R., Gisbert J.. Helmintofauna de Mustela putorius Linnaeus, 1758 (Carnivora: Mustelidae) en la península Ibérica [Helminths fauna of Mustela putorius Linnaaeus, 1758 (Carnivora: Mustelidae) in the Iberian Peninsula] BoII. Soco Hist. Nat. Balears. 1996;39:155–165. In Spanish. [Google Scholar]
  83. Torres J., Feliu C., Fernández-Morán J., Ruíz-Olmo J., Rosoux R., Santos-reis M., Miquel J., Fons R.. Helminth parasites of the Eurasian otter Lutra lutra in southwest Europe. J. Helminthol. 2004;78(4):353–359. doi: 10.1079/JOH2004253. [DOI] [PubMed] [Google Scholar]
  84. Torres J., Miquel J., Casanova J.C., Ribas A., Feliu C., Morand S.. Endoparasite species richness of Iberian carnivores: influences of host density and range distribution. Biodivers. Conserv. 2006;15:4619–4632. doi: 10.1007/s10531-005-5824-8. [DOI] [Google Scholar]
  85. Torres J., Miquel J., Fournier P., Fournier-chambrillon C., Liberge M., Fons R., Feliu C.. Helminth communities of the autochthonous mustelids Mustela lutreola and M putorius and the introduced Mustela vison in south-western France. J. Helminthol. 2008;82(4):349–355. doi: 10.1017/S0022149X08046920. [DOI] [PubMed] [Google Scholar]
  86. Vieira F.M., Munizpereira L.C., Lima S.S., Moraes neto A.H.A., Gonçalves P.R., Luque J.L. Crenosoma brasiliense sp. n. (Nematoda: Metastrongyloidea) parasitic in lesser grison, Galictis cuja (Molina, 1782) (Carnivora, Mustelidae) from Brazil, with a key to species of Crenosoma Molin, 1861. Folia Parasitol. (Praha) 2012;59(3):187–194. doi: 10.14411/fp.2012.026. [DOI] [PubMed] [Google Scholar]
  87. Vismanis K., Ozolins J. Proceedings VII International Otter Colloquium. Trebon: Czech Republic; 1998. 1998. Preliminary data on parasites of European otter in Latvia; pp. 374–378. March 14-19. 1998, pp. [Google Scholar]
  88. Weber J.M.. Gastrointestinal helminths of the otter, Lutra lutra in Shetland. J. Zool., Lond. 1991;224(2):341–346. doi: 10.1111/j.1469-7998.1991.tb04814.x. [DOI] [Google Scholar]
  89. Willemsen G.F.. A revision of the Pliocene and Quaternary Lutrinae from Europe. Scripta Geol. 1992;101:1–115. [Google Scholar]
  90. Zabala J., Zuberogoitia I., Martínez-Climent J.A. Site and landscape features ruling the habitat use and occupancy of the polecat Mustela putorius in a low density area: a multiscale approach. Eur. J. Wildl. Res. 2005;51(3):157–162. doi: 10.1007/s10344-005-0094-z. [DOI] [Google Scholar]
  91. Zabiega M.H.. Helminths of mink, Mustela vison, and muskrats, Ondatra zibethicus, in Southern Illinois. J. Helminthol. Soc. Wash. 1996;63(2):246–250. [Google Scholar]
  92. Zschille J., Heidecke D., Stubbe M.. Verbreitung und Ökologie des Minks - Mustela vison Schreber, 1777 (Carnivora, Mustelidae) - in Sachsen-Anhalt [Distribution and ecology of feral American mink Mustela vison Schreber, 1777 (Carnivora, Mustelidae) in Saxony-Anhalt (Germany)] Hercynia. 2004;37(1):103–126. [Google Scholar]

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