A Study of Oribatid Mites as Potential Intermediate Hosts of Anoplocephalid Tapeworms of Tatra chamois and Tatra marmots from the Tatra Mountains, Central Europe, and Report of a New Intermediate Host for Andrya cuniculi, the Parasite of Leporidae
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
VEGA 1/0043/19
Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic
PubMed
37109484
PubMed Central
PMC10144853
DOI
10.3390/life13040955
PII: life13040955
Knihovny.cz E-zdroje
- Klíčová slova
- Andrya cuniculi, Anoplocephalidae, Oribatida, Tatra Mountains, Tectocepheus velatus sarekensis, chamois, marmot, parasites,
- Publikační typ
- časopisecké články MeSH
Tatra chamois (Rupicapra rupicapra tatrica (Blahout 1972)) and Tatra marmot (Marmota marmota latirostris (Kratochvíl 1961)) are significant endemic subspecies of the subalpine and alpine ranges of the Tatra Mountains in Central Europe. In four studied localities in the range of their typical biotopes in Slovakia and Poland, we investigated intestinal parasites of Tatra chamois and Tatra marmots, with an emphasis on anoplocephalid tapeworms. We also studied the occurrence, species diversity, and abundance of oribatid mites as intermediate hosts thereof, and the prevalence of cysticercoid larval stages of anoplocephalid tapeworms in collected oribatids using morphological and molecular methods. Coprological analyses revealed the average positivity of Moniezia spp. in chamois faeces at 23.5% and Ctenotaenia marmotae in marmot samples at 71.1%, with significant differences between the localities under study. Morphological analyses determined the presence of cysticercoids in five oribatid species: Ceratozetes gracilis, Edwardzetes edwardsi, Scheloribates laevigatus, Trichoribates novus, and Tectocepheus velatus sarekensis. This is the first record of T. v. sarekensis as an intermediate host of anoplocephalid tapeworms, as well as the first report of Andrya cuniculi occurrence in the territory of the Tatra Mountains, confirmed also by molecular methods.
Administration of Tatra National Park Tatranská Lomnica 66 059 60 Vysoké Tatry Slovakia
Institute of Parasitology Slovak Academy of Sciences Hlinkova 3 040 01 Košice Slovakia
Tatra National Park Kuźnice 1 34 500 Zakopane Poland
University of Veterinary Medicine and Pharmacy in Košice Komenského 73 041 81 Košice Slovakia
Zobrazit více v PubMed
Mituch J. K helmintofaune raticovej zveri prežúvavej v TANAPe. Ceskoslov. Ochr. Prírody. 1969;8:239–250. (In Slovak)
Novacký M., Chovancová B. Symboly Tatier. In: Koutná A., Chovancová B., editors. Tatry–Príroda. Baset; Prague, Czech Republic: 2010. pp. 617–639.
Mituch J. Proceedings of Zborník Prác o Tatranskom Národnom Parku 16. Martin; Osveta, Slovakia: 1974. Helmintofauna aves and mammalia; pp. 43–64.
Mituch J., Hovorka J., Hovorka I., Tenkáčová I. Helminty a Helmintocenózy Raticovej Poľovnej Zveri v Ekologických Podmienkach Karpatského Oblúka. Helmintologický Ústav SAV; Košice, Slovakia: 1984. p. 81. (Phase: Final Report). (In Slovak)
Štefančíková A., Chovancová B., Hájek B., Dudiňák V., Šnábel V. Revision of chamois infection by lung nematodes under ecological conditions of national parks of Slovakia with respect to ongoing global climate changes. Helminthologia. 2011;48:145–154. doi: 10.2478/s11687-011-0022-6. DOI
Hurníková Z., Miterpáková M., Chovancová B., Jászayová A., Zwijacz-Kozica T. Pilot research on gastronitestinal parasites of Tatra chamois (Rupicapra rupicapra tatrica) Ann. Agric. Environ. Med. 2022;29:513–517. doi: 10.26444/aaem/155254. PubMed DOI
Ribarić P., Bujanić M., Šprem N., Kavčić K., Sindičić M., Konjević D., Martinković F. Book of Abstracts III, Proceedings of the International Rupicapra Symposium, Šprem, Nikica. Agronomski Fakultet Sveučilišta u Zagrebu; Makarska, Croatia: 2021. Gastrointestinal parasites of Alpine chamois (Rupicapra rupicapra rupicapra): Coprology vs. intestine examination; p. 6.
Hoby S., Schwarzenberger F., Doherr M.G., Robert N., Walzer C. Steroid hormone related male biased parasitism in chamois, Rupicapra rupicapra rupicapra. Vet. Parasitol. 2006;138:337–348. doi: 10.1016/j.vetpar.2006.01.028. PubMed DOI
Morrondo P., Vazquez L., Diez-Banos P. Parasitic infections of wild ruminants in Spain with special attention to roe deer and chamois. Parassitologia. 2010;52:155–158.
Stancampiano L., Serra S., Battelli G. Gastro-intestinal nematode infection in four Alpine chamois herds: Influence of host density on helminth egg output. Parassitologia. 2001;43:123–130. PubMed
Kalúz S., Ferenčík J. Pokalamitný Výskum v TANAP-e 2008. Geofyzikálny ústav SAV; Bratislava, Slovakia: 2009. Pôdne roztoče (Acari) kalamitných plôch vo Vysokých Tatrách; pp. 108–119.
Kocian J. Štíty a doliny. In: Koutná A., Chovancová B., editors. Tatry–Príroda. Baset; Prague, Czech Republic: 2010. pp. 45–186.
Weigmann G. Hornmilben (Oribatida): Acari, Actinochaetida. Goecke & Evers; Keltern, Germany: 2006. p. 520.
Subías L.S. Listado Sistemático, Sinonímico y Biogeográfico de los Ácaros Oribátidos (Acariformes: Oribatida) del Mundo. Graellsia. 60 (Número Extraordinario): 3-305. 17ª Actualización; 2004. Updated in 2020. [(accessed on 7 October 2022)]. p. 527. Available online: http://bba.bioucm.es/cont/docs/RO_1.pdf.
Katz A.D., Taylor S.J., Davis M.A. At the confluence of vicariance and dispersal: Phylogeography of carnicolous springtails (Collembola: Arrhopalitidae, Tomoceridae) codistributed across a geologically complex karst landscape in Illinois and Missouri. Ecol. Evol. 2018;8:10306–10325. doi: 10.1002/ece3.4507. PubMed DOI PMC
Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., von Haeseler A., Lanfear R. IQ-TREE 2: New models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 2020;37:1530–1534. doi: 10.1093/molbev/msaa015. PubMed DOI PMC
Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC
Tamura K., Stecher G., Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol. Biol. Evol. 2021;38:3022–3027. doi: 10.1093/molbev/msab120. PubMed DOI PMC
R Core Team . R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing; Vienna, Austria: 2022. [(accessed on 6 March 2023)]. Available online: https://www.R-project.org/
Reiczigel J., Marozzi M., Fabian I., Rozsa L. Biostatistics for parasitologists—A primer to Quantitative Parasitology. Trends Parasitol. 2019;35:277–281. doi: 10.1016/j.pt.2019.01.003. PubMed DOI
Wickham H., Averick M., Bryan J., Chang W., McGowan L.A., François R., Grolemund G., Hayes A., Henry L., Hester J., et al. Welcome to the tidyverse. J. Open Source Softw. 2019;4:1686. doi: 10.21105/joss.01686. DOI
Oksanen J., Simpson G.L., Guillaume F.B., Kindt R., Legendre P., Minchin P.R., O’Hara R.B., Simpson G.L., Solymos P. Vegan: Community Ecology Package. 2022. [(accessed on 7 March 2023)]. Available online: https://github.com/vegandevs/vegan.
Maechler M., Rousseeuw P., Struyf A., Hubert M. Cluster: “Finding Groups in Data”: Cluster Analysis Extended Rousseeuw et al. 2021. [(accessed on 7 March 2023)]. Available online: https://svn.r-project.org/R-packages/trunk/cluster/
Lüdecke D., Ben-Shachar M.S., Patil I., Waggoner P., Makowski D. Performance: An R Package for Assessment, Comparison and Testing of Statistical Models. J. Open Source Softw. 2021;6:3139. doi: 10.21105/joss.03139. DOI
Brooks M.E., Kristensen K., van Benthem K.J., Magnusson A., Berg C.W., Nielsen A., Skaug H.J., Maechler M., Bolker B.M. glmmTMB Balances Speed and Flexibility Among Packages for Zero-Inflated Generalized Linear Mixed Modeling. R J. 2017;9:378–400. doi: 10.32614/RJ-2017-066. DOI
Fox J., Weisberg S., Price B., Friendly M., Hong J. Effects: Effect Displays for Linear, Generalized Linear, and Other Models. 2022. [(accessed on 7 March 2023)]. Available online: https://CRAN.R-project.org/package=effects.
Denegri G.M. Review of oribatid mites as intermediate hosts of tapeworms of the Anoplocephalidae. Exp. Appl. Acarol. 1993;17:567–580. doi: 10.1007/BF00053486. DOI
Roczeń-Karczmarz M., Tomczuk K. Oribatid mites as vectors of invasive diseases. Acarologia. 2016;56:613–623. doi: 10.1051/acarologia/20164143. DOI
Tomczuk K., Grzybek M., Szczepaniak K., Studzińska M., Demkowska-Kutrzepa M., Roczeń- Karczmarz M., Zahrai A., Kostro K., Junkuszew A. Factors affecting prevalence and abundance of A. perfoliata infections in horses from south-eastern Poland. Vet. Parasitol. 2017;246:19–24. doi: 10.1016/j.vetpar.2017.08.027. PubMed DOI
Pacek S., Seniczak S., Graczyk R., Chachaj B., Seniczak A. Seasonal dynamics of mites (Acari) in pastures and meadows in Poland, with species analysis of Oribatida. Acarologia. 2020;60:668–683. doi: 10.24349/acarologia/20204395. DOI
Stunkard H.W. The life cycle of Moniezia expansa. Science. 1937;86:312. doi: 10.1126/science.86.2231.312.b. PubMed DOI
McAloon F.M. Oribatid mites as intermediate hosts of Anoplocephala manubriata, cestode of the Asian elephant in India. Exp. Appl. Acarol. 2004;32:181–185. doi: 10.1023/B:APPA.0000021795.02103.d0. PubMed DOI
Kassai T., Mahunka S. Studies on tapeworm in ruminants II: Oribatids as intermediate hosts of Moniezia species. Acta Veterina Hung. 1965;15:227–249. PubMed
Akrami M.A., Saboori A., Eslami A. Observations on oribatid mites (Acari: Oribatida) serving as intermediate hosts of Moniezia expansa (Cestoda: Anoplocephalidae) in Iran. Int. J. Acarol. 2007;33:365–369. doi: 10.1080/01647950708683699. DOI
Schuster R.K., Coetzee L. Cysticercoids of Anoplocephala magna (Euccestoda: Anoplocephalidae) experimentally grown in oribatid mites (Acari: Oribatida) Vet. Parasitol. 2012;190:285–288. doi: 10.1016/j.vetpar.2012.05.022. PubMed DOI
Ebermann E. Oribatiden (Oribatei, Acari) als Zwischenwirte des Murmeltier-Bandwurmes Ctenotaenia marmotae (Frölich, 1802) Parasitol. Res. 1976;50:303–312. (In German) PubMed
Ahaniazad M., Bagheri M., Roumi V., Akrami M.A. An efficient and non-destructive DNA extraction method for oribatid mites. Arch. Phytopathol. Plant Prot. 2018;51:187–196. doi: 10.1080/03235408.2018.1444003. DOI
Sattlerová-Štefančíková A. Kamzík a Jeho Parazitárne Ochorenia. Press Print, Parazitologický Ústav SAV; Košice, Slovakia: 2005. p. 124.
Mituch J. Správa o Helmintologickom Vyšetrení Niektorých Cicavcov z Oblasti TANAP-u: Záverečná Správa. Tatranská Lomnica: Výskumná Stanica a Múzeum. Helmintologický Ústav SAV; Košice, Slovakia: 1970. p. 2. (Phase: Final Report). (In Slovak)
Callait M.P., Gauthier D. Parasite adaptations to hibernation in Alpine marmots (Marmota marmota) In: Heldmaier G., Klingenspor M., editors. Life in the Cold. 11th International Hibernation Symposium. Springer; Berlin/Heidelberg, Germany: 2000. pp. 139–146.
Preleuthner M., Pinsker W., Kruckenhauser L., Miller W.J., Prosl H. Alpine marmots in Austria. The present population structure as a result of postglacial distribution history. Acta Theriol. 1995;3:87–100. doi: 10.4098/AT.arch.95-48. DOI
Preleuthner M., Canderola S., Lanfranchi P., Prosl H. Parasiten des Alpenmurmeltieres (Marmota marmota): Systematic, Entwicklung, Verbreitung. Neue Folge Nr. 1999;146:77–92.
Prosl H., Preleuthner M., Bergmann A. Endoparasites of Marmota marmota in the Tyrolian Alps. In: Basano B., Durio P., Gallo Orsi U., Macchi E., editors. Proceedings of the 1st International Syposium on the Alpine Marmota (Marmota marmot) and Genus Marmot. International Marmot Network; Torino, Italy: 1992. pp. 215–216.
Bassano B., Sabatier B., Rossi L., Macchi E. Parasitic fauna of the digestive tract of Marmota marmota in the western alps. In: Bassano B., Durio P., Gallo-Orsi U., Macchi E., editors. 1st International Syposium on the Alpine Marmota (Marmota marmot) and Genus Marmot. International Marmot Network; Torino, Italy: 1992. pp. 13–24.
Callait M.P. Marmotte alpine et endoparasites: Biologie des parasites et comparaison de l´infestation sur differents sites. In: Ramousse R., Le Berre M., editors. Proceedings of the 4éme Journée d´Étude sur la Marmotte Alpine. International Marmot Network; Lyon, France: 1997. pp. 53–58.
Gortázar C., Herrero J., García-Serrano A., Lucientes J., Luco D.F. Preliminary data on the parasitic fauna of the digestive system of Marmota marmota in the Western Pyrenees. In: Le Berre M., Ramousse R., Le Guelte L., editors. International Marmot Netwoirk. Biodiversity in Marmots; Moscow, Russia: 1996. pp. 105–108.
Krivopalov A., Abramov S., Akimova L., Barkhatova A., Gromov A., Konyaev S., Lopatina N., Sidorovich A., Vlasov E., Vlasenko P., et al. Molecular Characterization of Ctenotaenia marmotae (Frölich, 1802) Railliet, 1893 (Cyclophyllidea: Anoplocephalidae) Parasitizing Rodents of the Genus Marmota and Spermophilus from Eurasia. Diversity. 2022;14:531. doi: 10.3390/d14070531. DOI
Chovancová B. Súčasná situácia a perspektívy svišťa vrchovského tatranského v TANAP-e; Proceedings of the Conference Malá zver a jej Životné Prostredie; Košice, Slovakia. 1993; pp. 111–116. (In Slovak)
Tenora F., Koubkova B., Feliu C. Redescription of Andrya cuniculi (Blanchard, 1891) (Cestoda: Anoplocephalidae), a parasite of Oryctolagus ciniculus (Lagomorpha) in Spain. Folia Parasitol. 2002;49:50–54. doi: 10.14411/fp.2002.011. PubMed DOI
Foronda P., Castillo A.D., Abreu N., Figueruelo E., Piñero J., Casanova J.C. Parasitic helminths of the wild rabbit, Oryctolagus cuniculus, in different bioclimatic zones in Tenerife, Canary Islands. J. Helminthol. 2003;77:305–309. doi: 10.1079/JOH2003182. PubMed DOI
Rosický B., Krátochvíl J. Drobní savci Tatranského národního parku. Ochr. Přirody X. 1955;2:34–47. (In Czech)
Mošanský A. Proceedings of Zborník Prác o Tatranskom Národnom Parku 16. Martin; Osveta, Slovakia: 1974. Mammalia; pp. 267–294. (In Slovak)
Podobiński L. Stan zwierzyny w Tatrach w roku 1959 i w latach poprzednich. Wierchy. 1961;29:137–155.
Podobiński L. Zwierzęta Tatrańskiego Parku Narodowego w 1966, 1967 i wiosną 1962. Wierchy. 1968;37:260–270.
Haukisalmi V., Wickström L.M. Morphological characterisation of Andrya Railliet, 1893, Neandrya n.g. and Paranoplocephala Lühe, 1910 (Cestoda: Anoplocephalidae) in rodents and lagomorphs. Syst. Parasitol. 2005;62:209–219. doi: 10.1007/s11230-005-5499-2. PubMed DOI