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Helminth Fauna of Shrews (Sorex spp.) in LithuaniaRasa Binkienė aa Institute of Ecology of Vilnius University, Akademijos 2, LT-08412, Vilnius-21, LithuaniaVersion of record first published: 23 Jul 2012.

To cite this article: Rasa Binkienė (2006): Helminth Fauna of Shrews (Sorex spp.) in Lithuania, Acta Zoologica Lituanica,16:3, 241-245

To link to this article: http://dx.doi.org/10.1080/13921657.2006.10512738

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Acta Zoologica Lituanica, 2006, Volumen 16, Numerus 3

ISSN 1392-1657

241

HELMINTH FAUNA OF SHREWS (SOREX SPP.) IN LITHUANIA

Rasa BINKIENË

Institute of Ecology of Vilnius University, Akademijos 2, LT-08412 Vilnius-21, Lithuania. E-mail: zrasa@ekoi.lt

Abstract. The helminth fauna and helminth infection in two species of Sorex shrews (S. araneus andS. minutus) were studied in various parts of Lithuania. Altogether 34 species of helminths, representingtrematodes (5 species), cestodes (15) and nematodes (14), were recorded. The overall prevalence ofinfection of the common shrew (S. araneus) was 92.1% and that of the pigmy shrew (S. minutus) was91.1%. Most shrews were infected with cestodes (82.0% in S. araneus and 81.3% in S. minutus) andnematodes (83.9% and 85.4%, respectively), fewer with trematodes (21.1% and 6.3%, respectively).The total number of helminth species and the number of species per host were higher in S. araneus. Highprevalence of infection in shrews shows that these animals play a significant role in spreading of helminthspecies, especially cestodes and nematodes. Moreover, they are paratenic hosts of parasites of otheranimals, which are important to farming.Key words: Sorex araneus, S. minutus, trematode, cestode, nematode, prevalence, abundance, intensity

INTRODUCTION

Helminths of shrews (Sorex spp.) in Europe are wellinvestigated. There are some review articles on ces-todes (Vaucher 1971), Heligmosomidae nematodes(Vaucher & Durrette-Desset 1973) of shrews in Eu-rope and databases of the distribution of all living mul-ticellular European land and freshwater animals (FaunaEuropaea Web Service). However, data about helm-inths of shrews in Baltic countries are absent fromthese reviews. The only existing published informa-tion on helminths of shrews in Baltic countries is thefollowing: Cholodkowsky (1906) described one ces-tode species Ditestolepis diafana from Sorex araneusfrom Estonia and one paper (Þàsitytë 2001) providesdata on Sorex spp. cestodes in Lithuania. There are nodata on other helminths in Baltic countries.Two species of the genus Sorex (Insectivora, Soricidae),the common shrew (Sorex araneus L., 1758) and thepigmy shrew (S. minutus L., 1766), are widespread inLithuania (Balèiauskas et al. 1999). Therefore the in-vestigation into helminth fauna of these animals is im-portant for the study of the geographical distributionand biology of parasites. Moreover, it can have practi-cal application in veterinary medicine (of domestic ani-mals) as shrews can be intermediate or paratenic hostsof some helminths.The aim of the study was to investigate fauna of helm-inths of shrews, to estimate the distribution of theseparasites as well as their prevalence, intensity and abun-dance in Lithuania.

MATERIAL AND METHODS

Shrews were collected in six localities of Lithuaniabetween 1999 and 2005 (Fig. 1). A total of 184 speci-mens of shrews (139 specimens of common shrewsand 45 of pigmy shrews) were captured using snap orpitfall traps. Traps were inspected every day and thetrapped animals were dissected immediately by themethod of total helminthological dissection (Ivashkin et

Figure 1. Capture localities of Sorex araneus and S. mi-nutus shrews in Lithuania: 1 � Vilnius, 2 � Molëtai district,3 � Anykðèiai district, 4 � Radviliðkis district, 5 � Ðakiaidistrict, 6 � Ðilutë district.

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242Binkienë R.

al. 1971). The search for helminths was performedwith a light microscope under low magnification (×16).Before identification all helminths found in differentorgans of dissected animals were isolated and pre-served: nematodes in Barbagal�s solution or in 70%ethanol, cestodes � in 4% formalin solution or in 70%ethanol and trematodes � in 70% ethanol. For moredetailed morphological study temporary and permanenthelminth preparations were made and examined as de-scribed in Þàsitytë and Grikienienë (2002).

RESULTS

A total of 34 helminth species were recorded (Table1). The overall prevalence of infection of the commonshrew was 92.1% and that of the pigmy shrew was91.1%. Most shrews were infected with cestodes(82.0% in the common shrew and 81.3% in the pigmyshrew) and nematodes (83.9% and 85.4%, respec-tively), fewer with trematodes (21.1% and 6.3%, re-spectively). The majority of cestodes belong to thefamily Hymenolepididae (11 species), others to that ofDilepididae (4). The found nematodes belong to thefamilies: Angiostrongylidae (1), Capillariidae (4),Heligmosomidae (3), Strongyloididae (2), Ascarididae(2), Rhabditidae (1) and Spirocercidae (1). Only fivetrematode species of the families Brachylaimidae (1),Plagiorchiidae (3) and Panopistidae (1) were detected.The main localisation of helminths was the intestines,only Liniscus incrassatus localised in the bladder, Bra-chylaima fulvum, Rubenstrema exaspiratum, R. opis-thovitellinus, Aonchotheca kutori in the stomach,Hepatocestus hepaticus in the bile duct, Eucoleusoesophagicola in the oesophagus, Stephanskostrongylussoricis in lungs, Calodium soricicola in the liver, encap-

sulated larvae of Porrocaecum talpae on the intestineand mesentery, encapsulated Agammospirura minutis-sima larvae in muscles of the intestine and the diaphragm,Physocephalus sexalatus larvae in skeletal muscles.Two species of cestodes and five species of nema-todes were found only in larval stages (Table 1).There were some differences in helminth fauna of com-mon and pigmy shrews. The common shrew was in-fected with Pseudoleucochloridium soricis, R. opistho-vitellinus, Neoskrjabinolepis singularis, Ecrinolepistripartita, Spasskylepis ovaluteri, D. undula, P. para-doxa, H. hepaticus, C. soricicola, Longistriata trus,L. incrassatus, E. oesophagicola, P. talpae and P. sexa-latus helminths which were not detected in the pigmyshrew. Soricinia infirma and S. soricis were recordedonly in the pigmy shrew.Most of helminth infracommunities contained from oneto four species in the pigmy shrew and from two tosix species in the common shrew (Fig. 2). Infracom-munities of helminths of the pigmy shrew were com-monly composed of three species (22.5% of all inves-tigated communities) and those in the common shrew �of five species (18.8%). Only one common shrew wasinfected with fourteen species. The prevalence of in-fection with various helminth species in the commonshrew was between 0.7�47.5% and in the pigmyshrew � 2.2�57.8% (Table 1). The highest mean in-tensity and abundance was of U. prolifer cestode. Upto 1,666 specimens per host of this cestode were found.It is a small (584�829 µm in length) helminth localisedin the large intestine among intestinal villi.

DISCUSSION

The majority of helminths found during the study weremature. Some of them are stenoxenous and occur ex-clusively in Sorex spp., while all trematodes, cestodes:N. singularis, D. diaphana, U. prolifer, Monocercusarionis, and nematodes: C. soricicola, A. kutori ex-hibit eurixenous character and also parasitisedCrocidura and Neomys shrews. Only Parastrongyloideswinchesi, L. incrassatus and E. oesophagicola arecharacterised by low host specificity and are knownfrom Talpoidea, too (Ribas & Casanova 2006).Immature helminth species are not specific parasitesof shrews and get into shrews by accident. Dilepisundula, P. paradoxa and Porrocaecum ssp. are helm-inths of birds. Physocephalus sexalatus is of veteri-nary importance, because this nematode is known as aparasite of wild and domestic Suidae, peccary and,less commonly, tapirs, equines, cattle and lagomorphs(Anderson 2000).

Figure 2. Helminth infracommunities of shrews (Sorexaraneus and S. minutus) in Lithuania.

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243Helminth fauna of Sorex spp. in Lithuania

Table 1. Occurrence, prevalence, mean intensity and mean abundance of helminths recorded in Sorex araneus andS. minutus in Lithuania.

  Locality p% MI M AHelminth species

1 2 3 4 5 6 Sa Sm Sa Sm Sa Sm

Trematoda                        

Brachylaima fulvum (Dujardin, 1843) + + - - - - 2.9 2.2 5.25 7.00 0.15 0.16

Neoglyphe sobolevi Schaldybin, 1953 + + + - + - 3.2 2.2 12.60 303.00 0.45 6.73

Rubenstrema exaspiratum (Rudolphi, 1819) + + + + + + 5.4 6.7 7.69 18.00 0.72 1.20

Rubenstrema opisthovitellinus (Soltys, 1954) + + - - - + 3.6 - 1.40 - 0.05 -

Pseudoleucohloridium soricis Schaldybin, 1953 - - - - + - 2.9 - 2.50 - 0.07 -

Cestoda                        

Ditestolepis diaphana (Cholodkowsky, 1906) + - + - + + 11.5 20.0 63.25 57.89 7.28 11.58

Ekrinolepis tripartita (Zarnowski, 1955) + - + + + + 7.2 - 21.00 - 1.51 -

Lineolepis scutigera (Dujardin, 1845) + + + + - + 27.3 4.4 14.32 27.50 3.91 1.22

Neoskrjabinolepis schaldybini Spassky, 1947 + + + + + + 47.5 57.8 26.30 30.46 12.49 17.60

Neoskrjabinolepis singularis

(Cholodkowsky, 1912)+ - - - - + 1.4 - 6.50 - 0.09 -

Soricinia infirma (Zarnowski, 1955) - - - - - + - 2.2 - 29.00 - 0.64

Spasskylepis ovaluteri Schaldybin, 1964 + - + - + - 2.2 - 284.00 - 6.13 -

Staphylocystis furcata (Stieda, 1862) + + + + + + 15.1 6.7 3.71 6.67 0.56 0.44

Staphylocystoides stefanskii (Zarnowski, 1954) - - - + - + 1.4 8.9 7.50 44.00 0.11 3.91

Urocystis prolifer Villot, 1880 + - - - - + 21.6 17.8 270.73 135.13 58.43 24.02

Vigisolepis spinulosa (Cholodkowsky, 1906) + + + + + + 23.0 22.2 4.00 3.30 0.92 0.73

Dilepis undula (Schrank, 1788), larvae + - + + - + 10.1 - 3.50 - 0.35 -

Hepatocestus hepaticus (Baer, 1932) + - - - - - 0.7 - 5.00 - 0.04 -

Monocercus arionis (Siebold 1850) + + + + + + 40.3 4.4 7.45 2.50 3.00 0.11

Polycerus paradoxa (Rudolphi, 1802), larvae - - - - - + 0.7 - 57.00 - 0.41 -

Nematoda                        

Stephanskostrongylus soricis (Soltys, 1954) + + + - - + - 40.0 - 3.11 - 1.24

Aonchotheca kutori (Ruchlyadeva, 1964) + + + + + + 12.2 51.1 2.82 6.00 0.35 3.07

Calodium soricicola (Yokogawa &

Nishigori, 1924)+ - + - + - 5.0 - 2.29 - 0.12 -

Eucoleus oesophagicola (Soltys, 1952) + + + - + + 23.0 - 4.28 - 0.99 -

Liniscus incrassatus (Diesing, 1851) + + + + - + 19.4 - 9.15 - 1.78 -

Longistriata depressa (Dujardin, 1845) + + + + + + 45.3 40.0 8.30 1.22 3.76 0.49

Longistriata pseudodidas Vaucher et

Durette-Desset, 1973+ + + - + + 29.5 26.7 6.49 3.08 1.91 0.82

Longistriata trus Thomas, 1953 + - - - - + 8.6 - 9.67 - 0.83 -

Parastrongyloides winchesi Morgan, 1928 + + + + + + 41.7 15.6 8.05 1.57 3.36 0.24

Physocephalus sexalatus (Molin, 1860), larvae + - - - - - 0.7 - 12.00 - 0.09 -

Porrocaecum talpae (Schrank, 1788), larvae + - + - - + 3.6 - 9.60 - 0.35 -

Porrocaecum sp., larvae - - + - - + 10.1 2.2 3.00 1.00 0.30 0.02

Rhabditis sp., larvae + + + + - + 25.9 6.7 22.89 1.33 5.93 0.07

Agammospirura minutissima Sharpilo,

1976, larvae+ + + - - + 23.7 15.6 8.42 5.71 2.00 0.89

p% � prevalence of infection; MI � mean intensity; MA � mean abundance; Sa � Sorex araneus; Sm � S. minutus;1 � Vilnius (84 Sa, 21 Sm), 2 � Molëtai district (4 Sa, 2 Sm), 3 � Anykðèiai district (13 Sa, 3 Sm), 4 �Radviliðkis district (5 Sa, 1 Sm), 5 � Ðakiai district (9 Sa, 4 Sm), 6 � Ðilutë district (25 Sa, 13 Sm) (in bracketsthe numbers of dissected individuals); �+� � it was found; �-� � it was not found

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Rare helminth species are B. fulvum, P. soricis,N. singularis, Soricinia infirma, S . ovalutari,Staphylocystoides stefanskii, H. hepaticus and L. trus.Lineolepis scutigera, N. schaldybini, M. arionis,A. kutori, Longistriata depressa, L. pseudodidas andP. winchesi are common and widespread helminth spe-cies in Lithuania, Finland (Haukisalmi & Henttonen1998) and Karelia (Anikanova et al. 2001). In Bulgaria(Janèev & Stoykova-Hadjinikolova 1980) the samecestode species and the nematode A. kutori are domi-nant, but helminth fauna of shrews in Bulgaria differsfrom that in Lithuania and Finland in the domination ofother nematode species. According to Janèev andStoykova-Hadjinikolova (1980), nematodes of the ge-nus Longistriata were not found in Bulgaria andP. winchesi was recorded only in the common molewhile these helminth species were abundant in shrewsin Lithuania, Finland and Karelia.The prevalence of the found trematodes is low be-cause of their complicated life cycle. Neoglyphe soboleviuses snails Galba corvus Gmelin, 1788 and Lymnaeastagnalis (Linnaeus, 1758), and R. exaspiratum andR. opisthiovitellinus use the snail Planorbarius corneus(Linnaeus, 1758) as the first intermediate host and themosquito Culex modestus Ficalbi, 1890 as the secondintermediate host (Buðta & Naðincova 1991; Naðinco-va & Buðta 1999; Naðincova et al. 1989). That is thereason why these trematodes were found more fre-quently than B. fulvum and P. soricis. In the life cycleof the latter the snails Aegopinella epipedostoma(Fagot, 1879), Euconulus fulvus (Müller, 1774),Goniodiscus rotundatus (Müller 1774), Oxychylusorientalis Clessin, 1887 and Zonitoides nitidus(Müller, 1774) participate as intermediate hosts(Pojmanska 1961). Some differences in the distribu-tion of helminth species in the examined host specieswere recorded. Lineolepis scutigera and M. arionis arecommon in the common shrew but are rare in the pigmyshrew, while A. kutori is more common in the pigmyshrew than in the common shrew. Janèev (1974), whostudied helminth fauna of rodents and insectivores inBulgaria, got the same results. Stephanskostrongylussoricis is a dominant species and occurred only in thepigmy shrew, because it is a specific parasite of thepigmy shrew. However, this cestode was recordedfrom Neomys fodiens (Pennant, 1771) by Prokopiè(1959), but because of the specificity of this species,a mistake can possibly have occurred.There is some difference in infection levels betweencommon and pigmy shrews. The common shrewharbours more helminth species and has more speciesper host individual. Similar results have been reportedfrom Wales (Lewis 1968), Slovakia (Ðtefanèikova et

al. 1994), Moldavia (Andreiko 1973) and West-Siberia(Fedorov 1975). According to Hanski (1984), a largersize of the common shrew implies higher absolute foodrequirement (that should increase the colonisation rateof helminths), but Haukisalmi (1989) suggests that highinfection levels in the common shrew are due to eitherits generalised diet or high abundance, rather than toits large body size.High level of infection with helminths in shrews showsthat these animals play a significant role in spreadingof helminth species, especially of cestodes and nema-todes. Moreover, they are paratenic hosts of parasitesof other animals, which are important to farming.It is necessary to pursue further investigations of hel-minth fauna and its structure in other localities ofLithuania and other Baltic countries.

ACKNOWLEDGEMENTS

This study was supported by the grant from theLithuanian State Science and Studies Foundation(project no. C-03056).

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SOREX KIRSTUKØ HELMINTØ FAUNA LIETUVOJE

R. Binkienë

SANTRAUKA

Ávairiose Lietuvos vietovëse buvo tiriama dviejø kirstukørûðiø (Sorex araneus ir S. minutus) helmintø fauna, ðiøhelmintø rûðiø paplitimas, uþsikrëtimo ekstensyvumas,bei intensyvumas. Ið viso buvo rastos 34 helmintø rû-ðys, priklausanèios trematodams (5 rûðys), cestodams(15 rûðiø) ir nematodams (14 rûðiø). Paprastojo kirstuko(S. araneus) uþsikrëtimo intensyvumas buvo 92,1%, okirstuko nykðtuko (S. minutus) � 91,1%. Daþniausiaikirstukai buvo uþsikrëtæ cestodais (82,0% paprastøjøkirstukø ir 81,3% kirstukø nykðtukø) ir nematodais(83,9% ir 85,4%, atitinkamai), reèiau � trematodais(21,1% ir 6,3%, atitinkamai). Paprastuosiuose kirs-tukuose buvo rasta ne tik daugiau helmintø rûðiø, bet irdidesnis rûðiø kiekis viename individe. Aukðtas kirstukøuþsikrëtimas rodo, kad ðie gyvûnai vaidina svarbøvaidmená helmintø plitime, ypaè cestodø ir nematodø.Be to jie yra rezervuariniai ðeimininkai helmintø para-zituojanèiø kituose ðeimininkuose, kurie yra svarbûsgyvulininkystei.

Received: 25 April 2006Accepted: 18 August 2006

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