This section describes various features of the tapeworm fauna of shrews, rodents (particularly voles and lemmings) and carnivores in Finland. The mammalian tapeworms are among the most extensively studied parasites in Finland, and practically all of them have been subject to molecular systematic analysis of some form. By contrast, evidently no published DNA sequence data exist for tapeworms of fishes and birds from Finland, with the exception of Caryophyllaeides fennica (see Brabec et al. 2012, Scholz et al. 2014), Diphyllobothrium ditremum and D. latum (see Wicht et al. 2010).

One of the main patterns emerging from the present data is the seemingly unexplained absence in (northern) Fennoscandia of several mammalian tapeworms that have extensive distributions in the Holarctic region or in Eurasia.

There are six species of shrews (Soricidae) in Finland, five species of Sorex and the water shrew Neomys fodiens. According to the present checklist, Sorex shrews have 15 species of tapeworms, most of them hymenolepidids, parasitizing shrews in the adult stage [this figure excludes Dilepis undula (Schrank, 1788) and Polycercus sp., parasites of birds that do not reach full size and maturity in shrews]. The smaller and scarcer species of Sorex shrews (S. minutus with 6 species, S. caecutiens with 12 species) have more depauperate tapeworm assemblages than the larger ones, particularly when compared with the numerically dominant S. araneus (with 15 species) (see also Haukisalmi 1989). However, their faunas are overlapping in the sense that all the tapeworms of the smaller shrews also parasitize the larger ones. The only (partial) deviation to this pattern may be Staphylocystoides stefanskii (Żarnowski, 1954), which has been found most frequently from the pygmy shrew S. minutus in Finland (one record from S. araneus). On the other hand, S. stefanskii is known to parasitize six species of Sorex in Eurasia (Binkienė et al. 2011). The tapeworm fauna of the smallest and scarcest Sorex species, the least shrew S. minutissimus, is unknown in Finland.

The tapeworm fauna of Sorex shrews in Finland is very similar to that found elsewhere in Europe and western Eurasia. In Europe, there are only two species that have not been found from Finland, that is, Skrjabinacanthus jacutensis Spasskii & Morozov, 1959 and Soricinia soricis (Baer, 1928). Skrjabinacanthus jacutensis is a rare parasite of Sorex shrews with an extensive but very patchy distribution in Eurasia (Binkienė et al. 2011). It is possible that it occurs in Finland, but has not been found yet because of its rarity. The apparent absence of S. soricis in Finland may be due to the fact that it has been confused with Soricinia infirma (Żarnowski, 1955) (see Karpenko 1999).

Among the tapeworms of Sorex shrews, only Spasskylepis ovaluteri Schaldybin, 1964 can be regarded as a northern species; according to Binkienė et al. (2011) it has not been reported further south than Belarus in Europe, and it seems to have a northern distribution also elsewhere in Eurasia.

The molecular systematic analysis of Haukisalmi et al. (2010b) indicated that there is a Ditestolepis species in the taiga shrew Sorex isodon in Finland that is distinct from the type species Ditestolepis diaphana (Cholodkovsky, 1906) and related species representing other genera. Because there should not be other Ditestolepis species in Europe or western Eurasia (Binkienė et al. 2011), the cestode from S. isodon may be a previously unknown species. Alternatively, it may one of the poorly known Ditestolepis species described from Japan (see the Global Cestode Database; Caira et al. 2012).

The water shrews of the genus Neomys have an almost entirely separate tapeworm fauna when compared with the genus Sorex, although there is a number of scattered records of Sorex tapeworms parasitizing Neomys shrews (Binkienė et al. 2011). The tapeworm fauna of Neomys fodiens and N. anomalus in Europe comprise 15 species, all of them hymenolepidids (Binkienė et al. 2011, 2015), whereas only two tapeworm species are known from N. fodiens in Finland. One of these is typically a parasite of Sorex shrews [Vigisolepis spinulosa (Cholodkovsky, 1906)], and the other (Polycercus sp.) is a parasite of birds that accidentally infects shrews and other mammals (reported also from the raccoon dog Nyctereutes procyonoides in the present checklist). The specific identity of V. spinulosa from the water shrew has been confirmed by DNA sequences (Haukisalmi et al. 2010b).

The apparent absence of host-specific tapeworms of Neomys in Finland could be due to biased sampling of water shrews and restricted distribution of freshwater amphipod crustaceans (Segerstråle 1954), the intermediate hosts of tapeworms of water shrews (Georgiev et al. 2006). The absence of host-specific tapeworms in Neomys in Finland seems to follow the general pattern for other parts of the northern Europe (Binkienė et al. 2011). Binkienė et al. (2011) suggested that the reason for the absence or extreme rarity of host-specific tapeworms in Neomys in the north is the low abundance of the definitive hosts. However, the restricted/patchy distribution of the amphipod intermediate hosts and their low numbers in the diet of water shrews seems to be an equally plausible explanation.

Finland has a relatively diverse fauna of arvicoline rodents (Cricetidae), consisting of nine species of voles, including the introduced muskrat Ondatra zibethicus, and two species of lemmings.

In Finland, voles and lemmings have ten species of tapeworms parasitic in the adult stage, eight of them anoplocephalids, one catenotaeniid and one hymenolepidid cestode. The Finnish/northern European tapeworm fauna of arvicoline rodents can be classified into three main types: “endemics” of northenmost Europe (two species), species with a Holarctic distribution (one species) and species with extensive European/western Eurasian distribution (seven species).

Paranoplocephala kalelai (Tenora, Haukisalmi & Henttonen, 1985) and Lemminia fellmani (Haukisalmi & Henttonen, 2001), parasitizing voles of the genus Myodes (particularly the grey-sided vole M. rufocanus) and the Norwegian lemming Lemmus lemmus, respectively, appear to have distributions restricted to northern Fennoscandia. Based on the present knowledge, these species could be classified as the only endemic tapeworms of northern Europe.

The restricted distribution of P. kalelai seems curious, because its primary definitive host (M. rufocanus) has a continent-wide distribution in northern Eurasia. It is possible that P. kalelai has been misidentifed in earlier studies. For example, the extensive faunistical study of mammalian helminths in the north-west of the Ural mountains (Yushkov 1995) lists Aprostatandrya macrocephala (Douthitt, 1915), A. caucasica (Kirshenblat, 1938) and Paranoplocephala omphalodes (Hermann, 1783) as parasites of the grey-sided vole [the valid name of A. macrocephala is Paranoplocephala macrocephala (Douthitt, 1915) and A. caucasica is considered a junior synonym of P. omphalodes; see Haukisalmi et al. 2014]. Of these species, P. macrocephala is morphologically rather similar to P. kalelai (see Tenora et al. 1985a, Haukisalmi et al. 2007) and may have been confused with the latter. It is now known that P. macrocephala has a strictly North American distribution, parasitizing voles of the genus Microtus and geomyid rodents there (Haukisalmi and Henttonen 2003, Haukisalmi et al. 2004), although this name still appears as a parasite of arvicoline rodents in Eurasia. Thus, the true distribution of P. kalelai remains to be verified, but, based on the collections of the Beringian Coevolution Project (Hoberg et al. 2003, Cook et al. 2005), it does not occur in M. rufocanus in easternmost Siberia (Chukotka Peninsula and adjacent regions).

If the restricted northern distribution of P. kalelai is found to be real, this would support the idea that P. kalelai has diverged as a result of a host shift from a northern European Microtus lineage (most likely M. oeconomus) to the Fennoscandian subclade of M. rufocanus after its divergence from the Siberian M. rufocanus populations (Cook et al. 2004, Haukisalmi et al. 2007). This scenario is supported by two phylogenetic/phylogeographic analyses on tapeworms of the genus Paranoplocephala (see Haukisalmi et al. 2004, 2007).

Lemminia fellmani is known only from the Norwegian lemming L. lemmus (a Fennoscandian endemic) from the mountains of southern Norway (Finse, type locality) and from northern Finland (Lapland) (Haukisalmi and Henttonen 2001). However, a morphologically and genetically related, congeneric cestode occurs in Lemmus trimucronatus is Alaska (Haukisalmi et al. 2010b), but it is uncertain if it is conspecific with L. fellmani. No tapeworms have been found from the wood lemming Myopus schisticolor in Finland, although Lemminia gubanovi (Gulyaev & Krivopalov, 2003) occurs in this host in eastern Siberia (Gulyaev and Krivopalov 2003).

Paranoplocephala jarrelli Haukisalmi, Henttonen & Hardman, 2006 is known to parasitize the tundra/root vole Microtus oeconomus (and accidentally other Microtus species) from northern Finland to Alaska (Haukisalmi et al. 2004), therefore being the only tapeworm of Finnish rodents to have a Holarctic distribution, with the possible exception of L. fellmani (above). The conspecificity of P. jarrelli populations in northern Finland, Hungary, the Russian Far East (Magadan) and Alaska has been verified by molecular methods (Haukisalmi et al. 2004).

Among the seven Finnish rodent tapeworms with an extensive European/western Eurasian distribution, Anoplocephaloides cf. dentata (Galli-Valerio, 1905), Microcephaloides cf. variabilis (Douthitt, 1915), Microticola blanchardi (Moniez, 1891), Paranoplocephala omphalodes (Hermann, 1783) and Hymenolepis (s.l.) asymmetrica Janicki, 1904 are primarily parasites of Microtus voles, Catenotaenia henttoneni is a parasite of Myodes voles (M. glareolus and M. rutilus) and Eurotaenia gracilis (Tenora & Murai, 1980) is a host-generalist parasite of voles and lemmings.

Present data for the geographical distribution of tapeworms of the field vole Microtus agrestis in Fennoscandia (Fig. 2) show that the range of A. cf. dentata, M. cf. variabilis, M. blanchardi and E. gracilis extends to the northenmost Fennoscandia, whereas P. omphalodes and H. asymmetrica are absent from the truly northern regions. Of the latter two species, P. omphalodes has a more northerly distribution than H. asymmetrica. The absence of these species from northernmost Finland is primarily based on nearly 40 years’ monitoring of arvicoline rodents and their helminths in western Finnish Lapland by H. Henttonen and coworkers, although extensive helminth datasets have been gathered also from other northern localities in Finland. The absence of these two species from the north seems peculiar, because their main definitive host (M. agrestis) occurs in the whole of the Fennoscandia, and is often the numerically dominant rodent species in open habitats throughout its range (Myllymäki et al. 1977).

Figure 2. 

The geographical distribution of tapeworms of the field vole Microtus agrestis in Fennoscandia. All species except Hymenolepis (s.l.) asymmetrica (Hymenolepididae) represent the family Anoplocephalidae. Grey symbols, species absent; black symbols, species present. The number of voles examined for helminths in each locality varies considerably, but is usually more than ten (several hundred in Kilpisjärvi and Pallasjärvi in western Finnish Lapland).

It is noteworthy that no tapeworms of the genus Arostrilepis Mas-Coma & Tenora, 1997 (Hymenolepididae) have been reported from Finland or elsewhere from Fennoscandia, except for the finding of A. horrida (von Linstow, 1901) from the bank vole M. glareolus from southern Norway (Baruš et al. 1977) and Russian Karelia (Mozgovoj et al. 1966). Arostrilepis species are ubiquitous parasites of arvicolines (and sporadically other rodents) in the Holarctic region, their range encompassing the central and southern Europe. Of the 12 valid species of Arostrilepis, at least eight occur in Eurasia (see the Global Cestode Database; Caira et al. 2012).

Another Holarctic tapeworm species evidently missing from Fennoscandia is Anoplocephaloides lemmi (Rausch, 1952), a parasite of lemmings of the genus Lemmus in northern Siberia and North America. The absence of this species seems real, because hundreds of Norwegian lemmings have been examined for helminths in Finnish Lapland and southern Norway by H. Henttonen and coworkers. It is hard to propose any general explanation for the absence of Arostrilepis species in most of Fennoscandia, but the absence of A. lemmi and another host-specific, Holarctic tapeworm species of Lemmus spp. [Arostrilepis beringiensis (Kontrimavichus & Smirnova, 1991)] may be the result of the severe population bottle-neck experienced by L. lemmus in Fennoscandia during the the last glacial maximum (Fedorov and Stenseth 2001, Haukisalmi and Henttonen 2001, Haukisalmi et al. in press).

Hymenolepis diminuta (Rudolphi, 1819) (a parasite of Rattus spp.) and H. hibernia Montgomery, Montgomery & Dunn, 1987 (a parasite of Apodemus spp.) may also be listed as “missing” species, although there do not exist extensive helminthological studies for rats in Finland. The unverified record of H. “diminuta” from Apodemus flavicollis (Raitis 1968; no voucher specimen exists), may, however, represent the latter tapeworm species.

There are 14 species of terrestrial carnivores in Finland. The present study lists 17 tapeworm species parasitizing carnivores in the adult stage, Taeniidae (nine species) being the dominant element of the fauna. However, the taeniid fauna of Finnish carnivores should also include two additional species, Taenia martis and Versteria mustelae (parasites of mustelids), which have been found so far only as metacestodes from rodents. The metacestode of the latter species has also been found unexpectedly from the otter Lutra lutra. There are no published studies on tapeworms of mustelids in Finland.

Five of the Finnish carnivore tapeworms [Dipylidium caninum (Linnaeus, 1758), Taenia solium (Linnaeus, 1758), Echinococcus equinus, E. granulosuss.s., E. multilocularis Leuckart, 1863] are clearly imported parasites that are not transmitted in Finland. The identification of recent imported infections of taeniid metacestodes in humans is based on DNA sequences (Lavikainen 2005, A. Lavikainen, unpubl.).

Echinoccus multilocularis is one of the tapeworm species that is mysteriously absent from Finland, although it has a Holarctic distribution and the definitive hosts (red fox Vulpes vulpes and other canids, including the raccoon dog) and intermediate hosts (rodents) are present in Finland. In addition, Taenia crassiceps (Zeder, 1800), a parasite of foxes that occurs basically throughout the Holarctic region, has not been found in Finland despite very extensive long-term studies on helminths of rodents (intermediate hosts of T. crassiceps) in Finland (H. Henttonen et al., unpublished). The absence of E. multilocularis and T. crassiceps may due to the fact that the density of the red fox, their primary definitive host, is below an (unknown) critical density for successful transmission of the parasite, and/or due to the pronounced density fluctuations of arvicoline rodents in Finland (Henttonen and Haukisalmi 2000). However, E. multilocularis has recently appeared in Denmark and Sweden (Kapell and Saeed 2000, Osterman Lind et al. 2011, Wahlström et al. 2012), and is predicted to spread to Finland as well.

Taenia pisiformis, with canids (including dog) as definitive hosts and hares as intermediate hosts, has evidently disappeared from Finland. In the 1940–50s, T. pisiformis was still a very common parasite in the country, known as the “bladder worm disease” of hares (Lampio 1946, 1950). However, no metacestodes of T. pisiformis were found from hares in early 1980s (Soveri and Valtonen 1983), and a recent survey of Taenia tapeworms in wolves from Finland and Sweden based on molecular identification (Lavikainen et al. 2011) also failed to find it. It is clear that the hunters’ awareness of the transmission of the parasite (hare offal should not be fed to dogs) and anthelmintic teatment of hunting dogs have played a major role in the disappearence of this parasite, but do not completely explain it, because suitable wild hosts are still numerous in Finland.

Recently, molecular methods have had a revolutionary impact on taeniid systematics. For example, the application of DNA based methods has enabled distinction of more or less cryptic, new species of Taenia, including T. arctos, a parasite of bears (definitive host) and cervids (intermediate hosts) in Finland, Alaska and Canada (Haukisalmi et al. 2011, Catalano et al. 2014). Taenia arctos had previously been confused with other Taenia species, mainly with Taenia krabbei Moniez, 1879, but it was found to be a genetically and biologically distinct entity (Lavikainen et al. 2010). Recently, another new species of Taenia, with the lynx (Lynx lynx) as a definitive host and cervids as intermediate hosts, has been found in Finland based on the molecular identification of adults and metacestodes (V. Haukisalmi, A. Lavikainen et al., unpubl.).

One of the main patterns emerging from the present checklist and associated comparisons is that the tapeworm fauna of vertebrates in Finland is significantly less speciose than the corresponding fauna in other parts of Europe. The difference is mainly due to the low number of bird tapeworms in Finland.

Such a pronounced difference may be a real one or due to a number of confounding factors, including differences in latitude, available habitats (freshwater, marine, montane etc.), the number of host species present and the proportion of host species examined (adequately) for tapeworms. It is not possible to determine how these factors (interactively) determine the variation in tapeworm diversity in Europe, but the last factor probably explains most of the variation.

First, most of the tapeworms of vertebrates considered here have a wide European or western Eurasian (or more extensive) distribution, and are expected to occur in Fennoscandia, provided that their definitive and intermediate hosts are present. Therefore, latitude alone should not explain the differences in tapeworm diversity among regions. The availability of habitats is not a sufficient explanation either, because Finland is a long country stretching from the Baltic Sea (Gulf of Finland) to near the Arctic Ocean, and freshwater habitats (including thousands of lakes) are ubiquitous. Semi-montane landscape prevails in northern Finland (Lapland). The number of vertebrate host species certainly affects tapeworm diversity, and the high overall tapeworm diversity in the Iberian Peninsula is probably partly explained by this factor. However, there are no marked differences in vertebrate diversity between Slovakia, Poland and Finland, except that there are slightly fewer species of fishes and water birds in Slovakia because of the absence of marine habitats.

These patterns favour the idea that low tapeworm diversity in Finland is mainly due to insufficient sampling of vertebrates, particularly anseriform, podicipediform, charadriiform and passeriform birds. The tapeworm fauna of Poland, which is among the best known in Europe (Pojmańska et al. 2007), forms the most suitable model when predicting the true number of tapeworm species in Finland. The diversity of vertebrates is roughly equal in Poland and Finland, and there are no major faunistical differences either. In addition, Poland and Finland are both situated on the Baltic sea.

The tapeworms of fishes and mammals in Finland are relatively well known and the number of tapeworm species in these hosts is taken as such. In Poland, there are 172 species of tapeworms in birds, which is taken as the predicted number for the Finnish fauna. Based on this method, there should be ca. 270 species of tapeworms in Finland, instead of the 170 species listed in the present study.