Heligmosomidae Cram, 1927

Varodi, E. I., Malega, A. M., Kuzmin, Y. I. & Kornyushin, V. V., 2017, Helminths Of Wild Predatory Mammals Of Ukraine. Nematodes, Vestnik Zoologii 51 (3), pp. 187-202 : 192-201

Family Heligmosomidae Cram, 1927

28. Heligmosomum costellatum (Dujardin, 1845)

S i t e o f i n f e c t i o n: intestine.

Host: red fox (P = 0.6 %; I = 9; A = 0.05) in Kherson Region.

29. Heligmosomum sp.

S i t e o f i n f e c t i o n: intestine.

Host: red fox (P = 0.6 %; I = 1; A = 0.06) in Kyiv Region.

30. Heligmosomoides sp.

S i t e o f i n f e c t i o n: intestine.

Host: weasel (P = 16.7 % (1/6); I = 10; A = 1.67) in Zakarpattia Region.

Some species of nematodes were not found in the present study; however, they had been recorded as parasites of carnivorans in Ukraine by other authors. Eight of such species were reported by Kadenatsii (1957) in Crimea: Baylisascaris (= Ascaris) columnaris , Filaroides martis, Perostrongylus falciformis, Dirofilaria immitis , D. repens , Strongyloides stercoralis , Spirura rytipleuritis , Gnathostoma spinigerum . The latter species was also mentioned by Petrov (1941) as occurring in Ukraine. Besides, Rukhliadev (1948) reported on the parasitism of Filaroides bronchialis in the stone marten from Crimea.

Additionally, we studied more than 80 specimens of domestic dogs and found 8 nematode species; 6 of them occurred also in wild canids. In 10 domestic cats four nematode species were found, all of them parasitized wild felids and/or canids as well. The nematodes Dirofilaria repens (in dogs and cats) and D. immitis (in dogs) were found only in domestic carnivorans. These species had been collected by veterinary surgeons and passed for identification to the authors. Dirofilaria immitis was recently collected from the wolf and the red fox in Kyiv Region (Y. Yakovlev, unpublished personal communication).

The species U. stenocephala appeared to have the widest distribution in Ukraine. It was found in 11 administrative regions and in Crimea, i. e. in almost all studied localities. Besides, the species has the widest range of hosts; it parasitizes all four canid species occurring in Ukraine, and two species of mustelids. Toxascaris leonina is another wide-spread species occurring in 10 regions and in Crimea, though it is parasitic in the red fox and the wolf only. The both species are also common in domestic dogs and cats in Ukraine.

Aonchotheca putorii has rather diverse host range. It was found in 6 species of mustelids and in one canid host in 6 regions of Ukraine. The host range of E. aerophilus includes two species of Canidae and two mustelid hosts. Molineus patens also occurs in both canids (one species) and mustelids (three species), however, it is rather rare in the red fox, similarly to Ao. putorii . On the other hand, Cr. vulpis is common in the red fox and rarely infects the badger.

Wild felids appeared to be parasitized with only specific nematodes: Tc. mystax and An. tubaeforme . However, we can not exclude the possibility of the wildcat infection with the nematode species commonly occurring in domestic dogs and cats: Tx. leonina , Tc. canis , U. stenocerhala , and An. caninum , especially in the localities where the wildcats may contact the domestic cats and dogs.

Our studies were not evenly detailed on the whole territory of Ukraine. Rather comprehensive information was obtained mostly from northern and western parts of the country. The richest nematode fauna in the studied host group was observed in the region of Polissia — the forest zone. There we found 16 nematode species. Significant data were obtained in Kyiv Region (9 host species examined, 14 species of nematodes found) , and Zhytomyr Region (5 host species examined, 13 nematode species found). Lesser number of hosts (6 species) was studied in Chernihiv Region , where we found 7 species of nematodes. In other parts of Polissia, Volynska , Rivne and Sumy Regions, we examined only the red foxes and found 2–3 most common species of parasitic nematodes. In Zakarpattia Region , three species of carnivorans were examined, and three nematode species were found. Three species of nematodes were found in the red fox in Lviv Region.

In central part of Ukraine, 5 nematode species were found in the red fox in Cherkasy Region, 2 species parasitized this host in Poltava and Dnipropetrovsk Regions. In southern Ukraine, three species of nematodes were collected from the red fox and the wolf in Zaporizhzhia Region and Crimea. In Kherson Region, the studies were more detailed; 8 species of nematodes were found in 5 species of hosts .

Nematodes appeared to be the most common group of helminths parasitizing wild carnivorans in Ukraine. In total, the prevalence of nematode infection reached 78.4 %, with 30 species found. Cestodes and trematodes were less common: 65.4 % and 17 species, and 39.6 % and 11 species, correspondingly ( Kornyushin et al., 2011; Korol et al., 2016).

The co-occurrence of several nematode species in the same host individual was quite commonly observed. In the largest host species (wolf and red fox), up to 4–5 nematode species were found simultaneously parasitizing an individual host. The nematode parasites were often accompanied with cestodes and/or trematodes. In most cases, the nematode communities included U. stenocerhala , Tc. canis and Tx. leonina . In the present study, we observed three kinds of communities consisting of 5 nematode species: Tc. canis + U. stenocerhala + Cr. vulpis + E. aerophilus + P. plica (found twice); Tx. leonina + U. stenocerhala + Tr. vulpis + E. aerophilus + P. plica ; Tx. leonina + U. stenocerhala + Cr. vulpis + E. aerophilus + P. plica . Nematode communities consisting of four species were even more common; we found 7 kinds of such communities: Tc. canis + U. stenocerhala + Tr. vulpis + M. patens ; Tc. canis + U. stenocerhala + E. aerophilus + P. plica ; Tc. canis + Tx. leonina + Tr. vulpis + R. acus; Tc. canis + Cr. vulpis + E. aerophilus + P. plica ; Tx. leonina + U. stenocerhala + Tricichinella sp. + E. aerophilus ; Tx. leonina + U. stenocerhala + M. patens + E. aerophilus ; Tx. leonina + U. stenocerhala + E. aerophilus + P. plica .

One or two nematode species were usually found in each specimen of mustelid hosts. Only in the pine marten, three nematode species were twice observed simultaneously parasitizing the same host individual: Ao. putorii + P. mucronata + E. aerophilus and P. mucronata + E. aerophilus + Sk. petrovi .

Nematodes parasitic in the red fox were studied comprehensively. We obtained information on the helminths of this host from 13 administrative regions of Ukraine, including Crimea, and found 19 species of nematodes. The diversity of nematodes parasitizing the red fox may be related to the wide trophic spectrum of this predator. Taxonomic structure of the nematode communities of the red fox consists of several distinct groups of species differing by their prevalence and intensity of infection (fig. 1, A). Toxascaris leonina , one of the most common species in the region, is predominating in the community. Two species, U. stenocerhala and Tc. canis , compose a group of sub-dominants. The group of common species also consists of two species, P. plica and E. aerophilus . Thereby, the core of the nematode community in the red fox is composed of 5 species with the prevalence of infection larger than 10% and the mean intensity of 10 or more specimens per host. Five more species, R. afinis, Tr. vulpis , M. patens , C. vulpis , and Capillaria sp. , are assigned to the group of rare species, with prevalence of infection less than 10 % and variable intensity of infection. Four of them are typical parasites of the red fox; the status of Capillaria sp. can be hardly determined.

Each of other 7 species was found in the red fox only once. Five of them are occasional parasites of the host, though their status is different. Spirocerca arctica is rare in Ukraine, it was previously found once in Crimea ( Kadenatsii, 1957). Spirocerca lupi has not been reported from Ukraine yet, and Trichinella cf. spiralis was not exactly identified in the present study, since we examined the morphology of only 2 adult females from the host intestine and did not study the host muscles in search for the larval stages. However, the occurrence of Trichinella sp. larvae in the muscles of the red fox is commonly reported in Ukraine. As for Srt. erschowi , in Ukraine it parasitizes mostly the raccoon dog and occasionally infects the red fox. Aonchotheca putorii is a specific parasite of mustelids; its presence in the red fox is accidental. Two species, S. agraria and Heligmosomum sp. , are the common parasites of rodents. Their occurrence in the red fox may be explained by the ability to post-cyclic parasitism. A considerable part of rare species found in the red fox in the present study confirms the completeness of knowledge on the nematode communities of this host in the region.

general (fig. 2). We found 15 species of nematodes in this host group. Six of them also occurred in the red fox. Interestingly, 3 species, namely, U. stenocerhala , Cr. vulpis , and M. pastens , are common in the red fox and in the badger. The possible explanation to this is the fact that the fox often uses the badger’s borrows for living.

The nematode community of mustelids, similarly to that of canids, consists of 5 main groups. Pearsonema mucronata found in three host species is predominating with the prevalence of 46.9 %. Sub-dominant group consists of Ao. putorii (P = 28.1 %) from 6 host species and M. patens (P = 15.6 %) from three hosts. The group of common species includes three species with prevalence about 10 %: E. aerophilus , found in two host species, Str. mustelorum , Str. lutrae found in one host species each and U. stenocephala from the badger. Thus, the core of the nematode community in mustelids is composed of 6 species. Six more species fall into the category of rare species. Their prevalence of infection is about 3%, each of them was found only once in the present study. In this group, Skr. petrovi showed the highest intensity of infection (I = 145 in pine marten); the infection intensity of Skr. nasicola and Ph. sibirica was also rather high (13 and 10 in steppe polecat and in badger, correspondingly). Each of three other rare species was found with infection intensity of 1 or 2 specimens. Filaroides martis and Sp. arctica are specific parasites of mustelids. Crenosoma vulpis is specific to canids, though quite commonly infects mustelids. Therefore, all three species can not be considered as occasional parasites of Mustelidae . The remaining two species, namely, Sy. arvicola and Heligmosomoides sp. , are normally parasitic in rodents; their occurrence in mustelid hosts is considered as post-cyclic parasitism. The presence of nematodes of rodents in the digestive tract of mustelids is commonly reported in parasitological studies of this host group. For example, Turianin (1959) found Protospirura sp. simultaneously parasitizing voles and the weasel in Transcarpathian region.

Among the studied species, the pine marten had the richest fauna of nematode parasites: 6 species, including U. stenocerhala acquired from canids. Rather diverse community of nematodes was observed in the weasel: 5 species, including 2 post-cyclic parasites acquired from rodents.The stone marten and the badger each harboured 4 nematode species, the steppe polecat was infected with 3 species, the stoat and the otter were parasitized with 1 nematode species each.

According to our data and information from literature, Mustelidae in Ukraine harbour quite a diverse fauna of nematodes: 31 species from 17 families (table 3). Twelve species are common for both Mustelidae and Canidae , 10 of them were found in the badger. In this host, 19 nematode species were registered — more than in other mustelids. Rather numerous nematode species were found in the stone marten (12 species) and the pine marten (10 species), as well as in the steppe polecat and the weasel (8 nematode species in each host). From 2 to 4 species of nematodes are known to parasitize the stoat, the European and American minks and in the otter in Ukraine (table 3).

The nematodes found in separate species of carnivorans in the present study are listed below.

1. Canidae

Wolf: 1. Pearsonema plica ; 2. Eucoleus aerophilus ; 3. Trichuris vulpis ; 4. Crenosoma vulpis ; 5. Ancylostoma caninum ; 6. Uncinaria stenocephala ; 7. Toxocara canis ; 8. Toxascaris leonina ; 9. Pterygodermatites affinis .

Golden jackal: 1. Uncinaria stenocephala .

Red fox: 1. Pearsonema plica ; 2. Aonchotheca putorii ; 3. Capillaria sp. ; 4. Eucoleus aerophilus ; 5. Trichuris vulpis ; 6. Trichinella cf. spiralis ; 7. Strongyloides erschowi ; 8. Crenosoma vulpis ; 9. Molineus patens ; 10. Uncinaria stenocephala ; 11. Ancylostoma caninum ; 12. Toxocara canis ; 13. Toxascaris leonina ; 14. Spirocerca arctica ; 15. Sp. lupi ; 16. Pterygodermatites affinis ; 17. Syphacia agraria ; 18. Heligmosomum castellatum ; 19. Heligmosomum sp.

Raccoon dog: 1. Strongyloides erschowi ; 2. Trichuris vulpis ; 3. Uncinaria stenocephala .

2. Felidae

Wildcat: 1. Ancylostoma tubaeforme ; 2. Toxocara mystax .

Lynx: 1. Toxocara mystax .

3. Mustelidae

Pine marten: 1. Pearsonema mucronata ; 2. Aonchotheca putorii ; 3. Eucoleus aerophilus ; 4. Skrjabingylus petrovi ; 5. Uncinaria stenocephala ; 6. Filaria martis .

Stone marten: 1. Pearsonema mucronata ; 2. Aonchotheca putorii ; 3. Eucoleus aerophilus ; 4. Spirocerca arctica .

Weasel: 1. Aonchotheca putorii ; 2. Strongyloides mustelorum ; 3. Molineus patens ; 4. Syphacia arvicola ; 5. Heligmosomoides sp.

Stoat: 1. Aonchotheca putorii .

Steppe polecat: 1. Pearsonema mucronata ; 2. Skrjabingylus nasicola .

American mink: 1. Pearsonema mucronata ; 2. Aonchotheca putorii ; 3. Molineus patens .

Badger: 1. Crenosoma vulpis ; 2. Molineus patens ; 3. Uncinaria stenocephala ; 4. Physaloptera sibirica .

Otter: 1. Strongyloides lutrae .

Nematodes with complex life-cycles (biohelminths) generally predominated in the nematode communities of carnivorans in Ukraine, representing 11 of 17 families: Capillariidae , Dioctophymidae , Crenosomatidae , Filaroididae , Spiruridae , Physalopteridae , Gnathostomatidae , Rictulariidae , Filariidae , Onchocercidae , and Trichinellidae .

The intermediate hosts of these nematodes are terrestrial gastropods, insects (mostly beetles), and earthworms ( Anderson, 2000). These animals are common items and quite often a substantial part of the diet of most carnivorans. Less commonly the nematode larvae develop in aquatic invertebrates, crustaceans and oligochaetes, and the final hosts are infected passively with water drunk from natural water bodies. Dipteran insects are the intermediate hosts and vectors for the species of Filariidae and Onchocercidae .

Trichinellids have a particular type of life-cycle. They may exploit the same host individual as the final host (adult nematodes dwell in the host intestine) and the intermediate host (larval nematodes migrate in blood circulatory system and settle in muscles).

Nematodes with simple life-cycles (geohelminths) belong to five families: Trichuridae , Strongyloididae , Ancylostomatidae , Trichostrongylidae , and Ascarididae . Species of the latter family perform a complex migration in the final host, the larvae travel through the portal vein and the lung artery to the lungs. These nematodes may use rodents as the paratenic hosts. The geohelminths compose a core of nematode communities in large carnivorans: the wolf, the red fox and the raccoon dog.

According to previously published information and our data, up to 50 nematode species parasitize wild predatory mammals in Ukraine. Such a diverse nematode fauna identified for this host group indicates, in our opinion, that the knowledge on the nematode communities in Ukrainian carnivorans is quite comprehensive.

In the neighbouring countries, particularly in Belarus and Moldova, the nematodes of carnivorans were also well-studied. In the catalogue published by Merkusheva and Bobkova (1981), 23 species of nematodes are reported from wild carnivorans in Belarus. There, the nematodes of some host groups, particularly of Mustelidae , were studied more comprehensively than in Ukraine. Aonchothaeca mustelorum was not found in Ukraine, whereas it was reported from the pine marten and the American mink in Belarus. Ten species of nematodes, mostly common parasites of mustelids, were reported from the European polecat in Belarus, and only three species were found in this host in Ukraine. In the raccoon dog in Belarus, 10 nematode species were found, whereas only 5 species are known in Ukraine (3 species are common for both countries). In Ukraine, such widely distributed species as Tx. leonina , Tc. canis , P. plica , Ao. putorii , E. aerophilus have not been found in this host yet.

Twelve nematode species were found in the lynx in Belarus, and only 3 species are reported from this host in Ukraine. Toxocara mystax is common for both countries. Pearsonema (= Capillaria ) feliscati was reported from the lynx in Belarus, whereas in Ukraine it is known only from the domestic cat. Other nematodes are common parasites of various carnivorans.

Nematode communities in the brown bear have not been studied in Ukraine yet. There are only records of Trichinella britovi from this host. In Belarus, this species was apparently identified as Tr. spirallis s. l. Three more species were reported from the brown bear in Belarus: Baylisascaris (= Toxascaris ) transfuga (Rudolphi, 1819) , U. stenocerhala and Tc. canis . The former one is specific to the bear, whereas the two latter ones are widely distributed parasites of carnivorans. Presumably, these nematodes may infect the brown bear, the lynx and the raccoon dog in Ukraine as well, at least in the northern part of the country (Polissia).

Fifteen species of nematodes parasitic in wild carnivorans of Moldova are reported in the monograph by Andreiko (1973). The nematode communities of the red fox were comprehensively studied; 7 nematodes species were found. All of them are known to parasitize the red fox in Ukraine. One nematode species, An. caninum , was reported from the raccoon dog in Moldova. The wildcat harboured 4 nematode species, three of them ( A. tubaeformis , Tc. mystax , and Tr. spiralis ) are known from this host in Ukraine, whereas E. aerophilus was found in a number of other hosts in the country. Four species of nematodes were reported from the badger in Moldova. One of them, Cr. schulzi , has been never found in Ukraine. Each of other mustelid species (pine marten, stone marten, weasel) harboured one nematode species; all of them are known from these hosts in Ukraine. Information on the helminths fauna of carnivorans from the regions of Russia adjacent to Ukraine is summarized in several recent publications. Itin (2015) in the dissertation on parasites of Carnivora from North-Western Caucasus listed 51 helminth species, including 25 nematodes. Three of those species have not been recorded in Ukraine: Eu. bohmi from the red fox, Cr. petrowi from the pine and stone martens and the American mink, and Petrowispirura petrowi from the wildcat.

Information on the helminths of the red fox in the studies of Itin (2015) is comprehensive; it is based on examination of 127 host specimens. Seventeen species of nematodes were found. Some of those species were not registered in Ukraine, such as Eu. bohmi , or were found in hosts other than the red fox: Tc. mystax , G. spinigerum , and D. renale . The latter species appeared to be quite common in the red fox in Kuban region.

In a rather large material collected by Itin (2015) from the raccoon dog (56 specimens examined), 14 species of nematodes were found; whereas only 5 species are known from this host in Ukraine. Two species, Tr. spiralis s. l. and U. stenocephala appeared to be common parasites of this host in both regions; other nematodes parasitize different carnivoran hosts in Ukraine. Helminth fauna of the jackal was also well-studied due to examination of 60 host specimens. Thirteen nematode species were found, all typical for other canids, whereas in Ukraine it was only U. stenocephala that was collected from a single jackal examined. In 9 specimens of the wolf, 7 nematodes were identified, all known in Ukraine as well. Four mustelid species were parasitologically examined in Krasnodar Krai; helminths of the badger were more comprehensively studied based on 60 specimens of the host. Only 10 nematode species were found in the badger in this region, whereas in Ukraine we have identified 18 species; 8 species were common for both regions. An. caninum and D. repens have not yet been reported from the badger in Ukraine; the latter species rarely parasitizes mustelids. Of other nematodes infecting mustelid hosts in Krasnodar Krai, the infection of the American mink by Cr. petrowi and martens by A. columnaris is yet unknown in Ukraine.

Information on the parasites of the wildcat in Krasnodar Krai is based on examination of 12 host specimens; 9 nematode species were found. All of those, excepting P. petrowi , are known from Ukraine as well. However, only two species, Tc. mystax and Tr. spiralis s. l., were found to parasitize this host in Ukraine. Five more species were reported from domestic cats; Ao. putorii normally infects mustelids. Author’s information on the parasites of the coon ( Procyon lotor ) is of greatest interest, since this host has been introduced into the region. In 26 studied coons, 7 species of nematodes were found. All of them are common parasites of European carnivorans. In Ukraine, this mammal is rare and its parasites are unknown.

The most comprehensive information on the nematode communities of carnivorans from other neighbouring countries ( Poland, Czech Republic, Slovakia, Hungary, Romania) concerns the parasites of Canidae , mostly the wolf and the red fox.

Information on the helminths of carnivorans in Poland is summarized in the review by Pojmańska et al. (2007). Twenty-five species of nematodes are reported in the review. Thirteen of them are parasitic in Canidae , 9 in Mustelidae , 3 in Felidae . One species is reported from the brown bear. Majority of the nematodes registered in Polish carnivorans are widely distributed and common parasites of these animals; most of them are known from Ukraine as well. Eight nematode species occurring in Poland, however, have not been found in Ukraine yet, namely, Baylisascaris transfuga from the brown bear; Aelurostrongylus obstrusus , Ollulanus tricuspis , and Tc. cati parasitic in felids; Trichuris nitzshi , U. criniformis , and Ao. mustelorum from mustelids; and Eu. boehmi from the red fox.

Nematodes of the golden jackal were recently studied in Hungary (Takacs et. al., 2014); 20 host specimens were examined. Under the environmental conditions favourable for this host, it is parasitized by 16 species of helminths, including 9 nematode species. An. caninum , U. stenocephala and P. plica predominated in the nematode communities, with the prevalence of 40–45 % and comparatively high intensity, 65–166 parasite specimens per host. All nematodes reported from the jackal in Hungary are common parasites of wild canids and the domestic dog in Ukraine, excepting Angiostrongylus vasorum (Raillet, 1866) . The latter species is known as a widely distributed parasite of canids, occurring also along the lower part of the Don River and in Caucasian region. Presumably, this species may parasitize the golden jackal in Ukraine.

Previously we have reported on 19 species of nematodes parasitic in domestic dogs and cats in Ukraine ( Kornyushin and Varodi, 2010; Kornyushin et al., 2013). All of them parasitize wild carnivorans in the country. A number of these species have epizootological and epidemiological significance.

Trichinae are the most dangerous; they may cause human disease often diagnosed as mass “intestinal infection”. Wrong diagnostics and inappropriate treatment may lead to death. Previously the synanthropic foci of Tr. spiralis in domestic pigs were considered as existing independently from the natural foci. Other species of Trichinella were believed to form the latter type of foci, namely, Tr. nativa and Tr. britovi in Ukraine. They infect wild carnivorans: the wolf, the red fox, the raccoon dog, the brown bear, and a number of mustelid species, as well as the wild boar. The latter species is used as game animal, and people may acquire infection from its meat. However, Tr. spiralis appeared to infect the wolf and the red fox in natural habitats ( Didyk, 2012, 2013; Didyk et al., 2013). This fact confirms a possibility of exchange between natural and synanthropic foci of trichinellosis.

Human dirofilariosis is an emerging and fast-spreading disease in Ukraine. It is caused by D. repens and related mostly to synanthropic regions, where the dogs are the primary hosts of the nematode ( Pavlikovska et al., 2014). On the other hand, wild canids may bear the infection, and the contacts between the natural and synanthropic foci are quite possible due to the participation of blood-sucking mosquitoes ( Culicidae ) as vectors in the nematode transmission. Besides, the stray dogs in vicinities of human settlements may closely contact wild canids.

Human toxocarosis is caused by visceral larvae migrans of Tc. canis , a common parasite of domestic and wild carnivorans. Migrating larvae may settle in human lungs causing subacute pneumonia and bronchitis. Red foxes and wolfs support the existence of toxocarosis foci in Ukraine.

The risk of spread of nematodoses from wild carnivorans in natural habitats to urbanized territories is increased due to the existence of stray dog packs, which may migrate to natural ecosystems and return to human settlements. By doing this, they form and support a constant exchange channel for parasitic nematodes and other disease agents. The other threat is related to the continuing urbanization of the red fox and its occurrence in the outskirts of cities in Ukraine, similarly to other European countries. This exchange of diseases between natural and synanthropic populations is an important reason for constant monitoring of helminthoses of wild and domestic predatory mammals.