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On parasitic helminths of mammals living in the environs of Lake Balaton. I /
É v a M U R A I 1 , F e r e n c M É S Z Á R O S 1 a n d O t t ó S E Y 2
Zoological Department, Hungarian Natural History Museum, H-1088 Budapest, Baross u. 13. Hungary
'Department of Zoology, Pannon University of Agricultural Sciences, H-8361 Keszthely, Deák Ferenc u. 16. Hungary
(Received 21 September, 1992)
Abstract: A list of helminth parasites recovered from 256 wild mammals, mainly small mammals, in the environs of Lake Balaton (Keszthely Bay, Csókakői stream) is given. Thirty-six individuals of four Insectivora species, 135 individuals of six Muridae and 79 individuals of four Microtidae species, as well as three Carnivora (5 individuals) and one Ungulata species were examined. The helminths presented a total of 41 species (9 Trematoda, 18 Cestoda and 14 Nematoda), the infections rate was 42.5%.
Only few papers have been published on the parasitological examination of mammalian species of various regions. Our team published the helminth fauna of insectivorous and rodent communities from the following areas of the Carpathian basin: Hortobágy National Park -HNP - (Mészáros et al. 1981), Kiskunság National Park - KNP - (Murai et al. 1985), Bátorliget Nature Réserve - BNR - (Matskási et al. 1990), the Cergov Mountains in the Eastern Beskidek - Cergov Protected Area (CPA)-(Matskási 1984, Mészáros and átollmann 1984, Murai and Mészáros 1984), and a
This study was supported by a grant from the National Research Fund (OTKA1/3, No: 1419)
valley with subalpine conditions in the Vel'ka Fatra Protected Area (VFPA) -Lubochnianska dolina - (Murai et al. 1983). The last two samples are in the Western Carpathians, Slovakia. We have the possibility to compare faunisticdata and host-parasite relationships of the present sampling, Balaton shoreline region - Balaton Protected Area (BPA) - with the former ones. The aim of the present work was to study the parasitic helminths, recovered from mammals in the environs of Lake Balaton in connection with the research project involving mammalian communities in littoral territories of Lake Balaton and conducted at the Pannon University of Agricultural Sciences, Keszthely.
M A T E R I A L A N D METHODS
Animals were collected by students of the University in the valley of the Csókakői stream arising from the Keszthely Mountains, in different habitats (bank of the stream, wood, grazing ground, reeds). Trap setting for micromammalians was done 20 occasions with 50-100 pitfall traps between October 1990 and February 1992, except the summer months. The collections generally lasted 4-6 days. As regards their species composition, the samples contained four species of shrews (Soricidae, 36 individuals), six species of mice (Muridae, 135 individuals) and three species of voles (Microtidae, 40 individuals). Predators, including 3 foxes (Vulpes vulpes), 1 badger (Mêles mêles), 1 beech-martin (Martes foina) and one deer (Capreolus capreolus) were badged by the rifle club. Muskrats (Ondatra zibethicus, 22 individuals) were purchased from professional collectors. In 1989, Sey investigated muskrats (17 individuals) in Keszthely Bay and recorded two trematode species (Sey 1990). These findings were also included in the faunistical and helminthological analysis.
The dead animals were dissected in fresh condition. The helminths were fixed and preserved in 70 % ethyl alcohol. Whole mount preparations of trematodes and cestodes were stained with alum-carmine or iron-acetic-carmine. Nematodes were prepared for translucence in lactophenol. Rostellar hooks and eggs were observed in Berlese solution. Trematodes were identified by Sey, cestodes by Murai and Nematodes by Mészáros, using the above-mentioned literature as well as the papers of Vaucher and Hunkeler (1967), Vaucher (1971) and Genov (1984), respectively.
RESULTS A N D DISCUSSION
Mammalian species examined from the valley of Csókakői stream in the period 1990 through 1992 (ratio of examined and infected specimens are in parenthesis)
For the lack of a taxonomic revision elaborating the genera by uniform principles, the hymenolepidid species are discussed under s. I. gen. Hymenolepis
Hymenolepis fraterna (Stiles, 1906)
Host: Apodemus agrárius, four cases, 10.04.91 (2 host), 25.04.91, 30 01.92. -Location: small intestine. - Intensity: 1-11 specimens.
Host: Vulpes vulpes, two cases, 28.11.91. - Location: small intestine. - Intensity: 1-1 specimen.
SPIRURIDAE Oerley, 1885 - larva -
Host: Sorex minutus, two cases, 06.02.92, 11.02.92. - Location: body cavity. -
Intensity: 1-1 specimen.
Characterisation and comparative investigation of the helminth communities in the environs of Lake Balaton
Adult and larval forms of 39 helminth species (7 Trematoda, 18 Cestoda and 14 Nematoda) were recovered from 239 host specimens in the valley of Csókakő, and two Trematoda from 17 muskrats in the Keszthely Bay. 109 individuals (42.5%) of all examined mammals were infected by helminths. Only one specimen, Sorex araneus proved to be infected by four helminth species simultaneously. Three parasitic helminth species were found in one Clethrionomys glareolus and one Vulpes vulpes. One Sorex minutus, two S. araneus, one Mus musculus, two Apodemus agrárius, threes. flavicollis, two A. sylvaticus, one Pitymys subterraneus, one C. glareolus, two V. vulpes and one Martes foina were infected by two species of parasites at the same time.
The general intensity of infection of the mammals in the valley of the Csókakői stream proved to be low. A l l of the infected animals (107 individuals) contained only 648 helminths (5 h/ind.), which may be related to the absence of the summer samples.
Tables 1-3 summarize the helminth infections of the micromammalian families examined. A deficiency of the collected material was that it contained no summer samples. The prevalence of helminth invasions was also demonstrated by season, such as autumn, winter and spring, respectively.
Table 1 Prevalence of parasitic helminths in insectivorous species
T R E M A T O D A P. soricis - 1 (1:0:0) - - 1 (1:0:0) N. sobolevi - 2 (2:0:0) - - 2 (2:0:0) R. exasperatum - 1 (0:1:0) - 1 (1:0:0) 2(1:1:0) P. europaeus - 2 (2:0:0) - - 2 (2:0:0) C E S T O D A H. furcata 1 (0:1:0) 1 (0:0:1) - 2(0:1:1) H. spinulosa 1 (0:1:0) - - - 1 (0:1:0) H. shaldybini 1 (0:1:0) - - - 1 (0:1:0) H. uncinata - - - 4 (4:0:0) 4 (4:0:0) H. singularis - 2(1:1:0) - - 2(1:1:0) H. tiara - - 1 (1:0:0) 1 (0:1:0) 2(1:1:0) H. diaphana 1 (0:1:0) 1 (0:1:0) - - 2 (0:2:0) C. crassiscolex - 1 (1:0:0) - - 1 (1:0:0) N E M A T O D A
Host - parasite relations of mammalian communities in the territory of Lake Balaton (BPA) were compared with five other regions of the Carpathian basin: Hortobágy National Park (HNP), Kiskunság National Park (KNP), Bátorliget Nature Reserve (BNR), Cergov Mts (CPA), Lubochna Valley (VFPA).
Table 4 summarizes the species composition of micromammalian synusium and the ratio of infected ones. The number of host specimens investigated was between 159 and 359 (except in the sample from Lubochna, which comprised 65 small mammals only), the rate of helminth infections was 42,60, 32, 53, 87 and 74%, respectively.
We presented a cumulative list of helminth species occurring in the Balaton area, and the hosts of each parasitic worm in all territories were investigated (Table 5). It is remarkable that the host specificity of helminths (at generic or family level) was the major factor influencing the species composition in the various localities. E.g. among the 41 parasitic worm species of the Balaton area three trematodes of muskrats occurred only in Balaton samples, because these hosts were hardly investigated in
Table 2 Prevalence of parasitic helminths in murid species
R. norv. M. muse. A agrar. A micr. A sylv. A. flav. Total
T R E M A T O D A P. elegáns - - - - - 2 (0:0:2) 2 (0:0:2) E . revolutum 1 (1:0:0) - - - - - 1 (1:0:0) C E S T O D A H . fraterna - - 4 (0:1:3) - - - 4 (0:1:3) N E M A T O D A H . polygyrus - 3 (0:0:3) 2 (0:0:2) 1 (0:1:0) 14 (1:9:4) 10 (2:8:0) 30 (3:18:9) S. agraria - - 4 (3:1:0) - - - 4 (3:1:0) S. frederici - - 1 (0:0:1) - 1 (1:0:0) 2(1:1:0) 4(2:1:1) S. stroma - 1 (0:0:1) 1 (1:0:0) - 3(1:0:2) 8 (2:6:0) 13 (4:6:3) S. obvelata - 7 (5:0:2) - - - - 7 (5:0:2) R. proni - - 1 (0:1:0) - - - 1 (0:1:0)
* autumn winter spring
other territories. Four nematode of predators: Eucoleus aerophilus, Paersonemaplica, Molineuspatens and Uncinaria criniformis occurred only in BPA, but this finding is not suitable for faunistical comparison.
Table 3
Prevalence of parasitic helmints in microtid species
O. zibethicus P. subterraneus C. glareolus M. arvalis Total
T R E M A T O D A P. pharyngeatum 4(0:0:4) - - - 4(0:0:4) C E S T O D A C. cricetorum - - 8(2:4:2) - 8(2:4:2) Adentata - 1(0:0:1) - - 1(0:0:1) P. omphalodes - - 8(0:8:0) - 8(0:8:0) T. taeniaeformis larva - 1(0:0:1) - - 1(0:0:1) T mustelae larv. - - 1 (0:1:0) - 1 (0:1:0) N E M A T O D A H. polygyrus - - 1(0:1:0) - 1(0:1:0) T. muris - - 2(0:0:2) - 2(0:0:2)
• * * * *
autumn, winter, spring, Sey (1989) collected in the Keszthely Bay 17 exs of Ondatra zibethicus and recorded two Trematoda species: Skrjabinoplagiorchis ondatrae (Andrejko, 1965) and Troglotrema srebarni Genov, 1964. These findings were included in the faunistical evaluation of the Balaton area, too
Table 4 Number of small mammals examined/infested in various localities
Occurrence of helminths and hosts in various localities
BPA HNP KNP BNR CPA VFPA
T R E M A T O D A P.-leuco. soricis S.a* - - S.ar + N.an - -Neogl. sobolevi S.ar S.ar - - - -Rub. exaspérât. S.ar + C.le S.m + A m i S.ar + C.le S.ar + S.m S.ar S.ar Panop. eur. S.ar - - - - -Plag, elegáns A.fl A.fl - Aag - -S.-plag, ondat. O.zib - - - - -Echin. revol. Rat - - - - -Trogl. srebarni O.zib - - - - -Psil. pharyng. O.zib - - - - -C E S T O D A Cat., cricet. ci.g - - - ci.g -Anopl. dentata P.s - - - M.ar + P.st -P.. omphalodes Cl.g M.ar. M.ar Cl.g ci.g P.st Hym. fraterna A a g - M.min - - -Hym. furcata S.ar + S.m S.ar S.ar + S.m - S.ar S.ar Hym. spinulosa S.m S.ar - - S.ar -Hym. shaldyb. S.m S.ar -1- S.m - S.ar S.ar S.ar Hym. uncinata C.le - C.le - - -Hym. singularis S.ar S.ar S.ar - - -Hym. tiara C.le + N.fo - - - N.fo -Hym. diaph. S.ar + S.m S.ar S.ar S.ar - S.ar C. crassiscolex S.ar S.ar S.ar S.ar S.ar S.ar M. lineatus Vulp - S.ar - S.ar -T. hydatigena Cap - - - - -T taeniaeformis Pst Af l + Mu Afl + Mu + M.ar Afl A f l + P.st -T crassiceps Vul - M.ar - - -T. mustelae Cl.g Cr + M.niv M.ar Cl.g + Pst + Mniv Cl.g + Rst P.st T. martis M.fo - - - Cl.g -
Table 5 (continued)
Occurrence of helminths and hosts in various localities
BPA HNP KNP B N R CPA V F P A
N E M A T O D A Vul* E . aerophilus Vul* - - - - -
Paers. plica Vul - - - - -Cal. soricic. S.ar + N.fo - - S. ar - -T muris Cl.g M.ar M.ar - - -H . polygyrus CLg + 4 Aspp + Mu. AflA.mi AmiA^y+Mu Afl, Ami A f l A f l S. agraria Aag Aag - Aag - -S. frederici Aag,Afl>Asy Afl,Ami - - A f l A f l S. stroma AagA-flA-sy +Mu A.fl.Ami A f l - - -S. obvelata Mu Mu Mu - - -
* C.le - Crocidura leucodon; C s u - C. suaveolens; N.an - Neomys anomalus; N.fo - N. fodiens; S.ar - Sorex araneus; S.m - S. minutus; A a g - Apodemus agrárius; A f l - A flavicollis; A m i - A microps; A sy - A sylvaticus; A spp - Apodemus species; Mu - Mus spp; Rat - Rattus spp; M.min - Micromys minutus; Cric - Cricetus cricetus; Cl.g - Clethrionomys glareolus; M.ar - Microtus arvalis; Rst - Pitymys subterraneus; 0.zib - Ondatra zibethicus; Vu - Vulpes vulpes; Mel - Mêles mêles; M.niv - Mustela nivalis; M.fo - Martes foina; Cap - Capreolus capreolus
The number of species common in our study site and in five other territories, as well as the number of additional species in each area, are demonstrated in Table 6. Compared with the ecosystems studied earlier, the helminth fauna of Lake Balaton shows the greatest similarity to that of Hortobágy and Kiskunság (with 18 and 17 common species, respectively). According to our data summarized in Table 6, the Jaccard index (per cent of species identity = the number of identical species found in two habitats, divided by the total number of species present in the two localities) obtained for Bátorliget is in many respects more similar to the mountain faunas which, however, contains many mountain elements (among others also Carpathian en-demisms and species new for the science). When analising the samples, the different abundance in species of the six sites is demonstrable.
Table 6
Similarities and differences of the helminth fauna in the regions investigated
BPA HNP KNP BNR CPA V F P A
T R E M A T O D A 4 5 3 2 1 1 3 4 1 3 1 0 C E S T O D A 17 0 9 6 11 6 6 4 12 13 6 9 N E M A T O D A 8 2 6 10 5 7 3 7 2 17 2 6 Total 29 7 18 18 17 14 12 15 15 33 9 15 Jaccard index (%) 0.25 0.25 0.19 0.18 0.15
Number of helminth species occurring simultaneously, Number of additional spp, Species identity in relation to the BPA
Considering that the extension of the collecting period to the summer season wil l increase the number of host species examined, the following well-known helminths are to be recovered: a trematode, Rubenstrema opisthovitellinum (Soltys, 1954), two cestodes of insectivorous mammals: Hymenolepis scutigera (Dujardin, 1845) and H. globosoides (Soltys, 1954); four cestodes of rodents: Hymenolepis horrida (Linstow, 1901), H. asymmetrica Janicki, 1904, Catenotaenia pusilla (Goeze, 1782) and Skrja-binotaenia lobata Baer, 1925; three nematodes of shrews: Capillaria kutori (Ruchl-jadeva, 1946), C. incrassata (Diesing, 1851), Eucoleus oesophagicola (Soltys, 1952) and Longistriata spp, as welll as three nematodes of rodents: Heligmosomoides laevis (Dujardin, 1845), Heligmosomum costellatum (Dujardin, 1845) and Syphacia nigeriana (Baylis, 1928) may occur in the environs of Lake Balaton, too.
Murai E . , Mészáros F. és Sey O.: A Balaton környékén élő emlősök belső-élősködő férgei. I.
A Keszthelyi Pannon Agrártudományi Egyetem Állattani Tanszékén a Balaton parti zónájában élő gerincesek parazitológiai vizsgálata folyik. 1990 őszétől 1992 tavaszáig a Keszthelyi hegységben eredő Csókakői patak völgyében 20 alkalommal végeztek csapdázást. Négy cickányfaj 36 egyede, hat egérféle 135 és négy pocokféle 62 példánya, továbbá öt ragadozó és egy őz került parazitológiai vizsgálatra. Sey (1990) a Keszthelyi öbölben 17 pézsmapockot vizsgált, ezekből 2 faunára új trematoda-fajt közölt. Vizsgálati anyagunkban 41 belső-élősködő féreg (9 métely, 18 galandféreg és 14 fonálféreg) ivarérett vagy lárvastádiumát azonosítottuk. A 256 gazdaállat közül 109 volt fertőzött (42,5 %) . Az emlősökben a féreg-fertőzöttség intenzitása viszonylag alacsony volt (5 féreg/gazda). A balatonkörnyéki parazita féregfaunát összehasonlítottuk további öt, a Kárpát-medence területén korábban vizsgált terület adataival (Hortobágy, Kiskunság, Bátorliget, Csergő-hegység és Lubochna-dolina). A balatonkörnyéki kisemlősök parazitái a Hortobágy és a Kiskunság féregfaunájával mutatnak közelebbi rokonságot.
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