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Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe

Published online by Cambridge University Press:  24 February 2011

GABRIELA HRČKOVA ,
MARTINA MITERPÁKOVÁ ,
ANNE O'CONNOR ,
VILIAM ŠNÁBEL  and
PETER D. OLSON
GABRIELA HRČKOVA*
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
MARTINA MITERPÁKOVÁ
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
ANNE O'CONNOR
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
VILIAM ŠNÁBEL
Affiliation:
Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic
PETER D. OLSON
Affiliation:
Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK
*
*Corresponding author: Parasitological Institute of the Slovak Academy of Sciences, Hlinkova 3, 040 01 Košice, Slovak Republic. Tel: +421 55 633 4455. Fax: +421 55 633 1414. E-mail: [email protected]
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Summary

Here we examine 3157 foxes from 6 districts of the Slovak Republic in order to determine for the first time the distribution, prevalence and identity of Mesocestodes spp. endemic to this part of central Europe. During the period 2001–2006, an average of 41·9% of foxes were found to harbour Mesocestoides infections. Among the samples we confirmed the widespread and common occurrence of M. litteratus (Batsch, 1786), and report the presence, for the first time, of M. lineatus (Goeze, 1782) in the Slovak Republic, where it has a more restricted geographical range and low prevalence (7%). Using a combination of 12S rDNA, CO1 and ND1 mitochondrial gene sequences together with analysis of 13 morphometric characters, we show that the two species are genetically distinct and can be differentiated by discrete breaks in the ranges of the male and female reproductive characters, but not by the more commonly examined characters of the scolex and strobila. Estimates of interspecific divergence within Mesocestoides ranged from 9 to 18%, whereas intraspecific variation was less than 2%, and phylogenetic analyses of the data showed that despite overlapping geographical ranges, the two commonly reported European species are not closely related, with M. litteratus more closely allied to North American isolates of Mesocestoides than to M. lineatus. We confirm that morphological analysis of reproductive organs can be used to reliably discriminate between these often sympatric species obtained from red foxes.

Keywords

MesocestoidesVulpes vulpes12S rDNACO1ND1Slovakia
Type
Research Article
Information
Parasitology , Volume 138 , Issue 5 , April 2011 , pp. 638 - 647
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Caruso, K. J., James, M. P., Fisher, D., Paulson, R. L. and Christopher, M. M. (2003). Cytological diagnosis of peritoneal cestodiasis in dogs caused by Mesocestoides sp. Veterinary Clinical Pathology 32, 50–60.CrossRefGoogle ScholarPubMed
Crosbie, P. R., Boyce, W. M., Platzer, E. G., Nadler, S. A. and Kerner, C. (1998). Diagnostic procedures and treatment of eleven dogs with peritoneal infections caused by Mesocestoides spp. Journal of the American Veterinary Medical Association 213, 1578–1583.CrossRefGoogle ScholarPubMed
Crosbie, P. R., Nadler, S. A., Platzer, E. G., Kerner, C., Mariaux, J. and Boyce, W. M. (2000). Molecular systematics of Mesocestoides spp. (Cestoda: Mesocestoididae) from domestic dogs and coyotes (Canis latrans). The Journal of Parasitology 86, 350–357.CrossRefGoogle ScholarPubMed
Dalimi, A., Sattari, A. and Motamedi, G. (2006). A study on intestinal helminths of dogs, foxes and jackals in the western part of Iran. Veterinary Parasitology 142, 129–133.CrossRefGoogle Scholar
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214–221.CrossRefGoogle ScholarPubMed
Drummond, A. J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Sturrock, S., Thierer, T. and Wilson, A. (2010). Geneious ver. 5.0, available from www.geneious.com.Google Scholar
Duscher, G., Pleydell, D., Prosl, H. and Joachim, A. (2006). Echinococcus multilocularis in Austrian foxes from 1991 until 2004. Journal of Veterinary Medicine Series B 53, 138–144.CrossRefGoogle ScholarPubMed
Eleni, C., Scaramozzino, P., Busi, M., Ingrosso, S., D'Amelio, S. and De Liberato, C. (2007). Proliferative peritoneal and pleural cestodiasis in a cat caused by metacestodes of Mesocestoides sp. Anatomohistopathological findings and genetic identification. Parasite 14, 71–76.CrossRefGoogle Scholar
Etges, F. R. (1991). The proliferative tetrathyridium of Mesocestoides vogae sp. n. (Cestoda). Journal of the Helminthological Society of Washington 58, 181–185.Google Scholar
Foronda, P., Riviero, A. P., Morales, M. A. S., Kabdur, A., González, A. C., Ricalde, M. A. Q., Feliu, C. and Valladares, B. (2007). First larval record of Mesocestoides in carnivora of Tenerife (Canary Islands). The Journal of Parasitology 93, 138–142.CrossRefGoogle ScholarPubMed
Fuentes, M. V., Galán-Puchades, T. and Malone, J. B. (2003). A new case report of human Mesocestoides infection in the United States. American Journal of Tropical Medicine and Hygiene 68, 566–567.CrossRefGoogle ScholarPubMed
Georgiev, B. B. and Kornyushin, V. V. (1994). Family Paruterinidae Fuhrmann, 1907 (senus lato). In Keys to the Cestode Parasites of Vertebrates (ed. Khalil, L. F., Jones, A. and Bray, R. A.), pp. 559–584. CAB International, Wallingford, UK.Google Scholar
Gubány, A. and Eszterbauer, E. (1998). Morphological investigation of Mesocestoides (Cestoda, Mesocestoididae) species parasitizing Vulpes vulpes in Hungary. Miscellanea Zoologica Hungarica 12, 11–19.Google Scholar
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hegglin, D., Bontadina, F., Gloor, S., Romig, T., Deplazes, P. and Kern, P. (2008). Survey of public knowledge about Echinococcus multilocularis in four European countries: Need for proactive information. BMC Public Health 8, 247.CrossRefGoogle ScholarPubMed
Jančev, J. (1986). Morphology, taxonomy and distribution of the species of genus Mesocestoides Vaillant, 1863 in Bulgaria. Helminthology (Sofia) 21, 45–65.Google Scholar
Kapel, C. M. O. and Nansen, P. (1996). Gastrointestinal helminths of arctic foxes (Alopex Lagopus) from different bioclimatological regions in Greenland. The Journal of Parasitology 82, 17–24.CrossRefGoogle ScholarPubMed
Králová-Hromadová, I., Štefka, J., Špakulová, M., Orosová, M., Bombarová, M., Hanzelová, V., Bazsalovicsová, E. and Scholz, T. (2010). Intra-individual internal transcribed spacer 1 (ITS1) and ITS2 ribosomal sequence variation linked with multiple rDNA loci: a case of triploid Atractolytocestus huronensis, the monozoic cestode of common carp. International Journal for Parasitology 40, 175–181.CrossRefGoogle ScholarPubMed
Khalil, L. F., Jones, A. and Bray, R. A. (Eds.) (1994). Keys to the Cestode Parasites of Vertebrates. CAB International, Wallingford, UK.CrossRefGoogle Scholar
Kinčeková, J., Hrčková, G., Bober, J., Vrzgula, A., Szabadošová, V., Bohuš, P. and Zachar, M. (2008). A rare case of alveolar echinococcosis in a 14-year-old child. Helminthologia 45, 28–31.CrossRefGoogle Scholar
Literák, I., Olson, P. D., Georgiev, B. B. and Špakulová, M. (2004). First record of metacestodes of Mesocestoides sp. in the common starling (Sturnus vulgaris) in Europe, with an 18S rDNA characterization of the isolate. Folia Parasitologica 51, 45–49.CrossRefGoogle ScholarPubMed
Literák, I., Tenora, F., Letková, V., Goldová, M., Torres, J. and Olson, P. D. (2006). Mesocestoides litteratus (Batsch, 1786) (Cestoda: Cyclophyllidea: Mesocestoididae) from the red fox: morphological and 18S rDNA characterization of European isolates. Helminthologia 43, 191–195.CrossRefGoogle Scholar
Littlewood, D. T. J., Waeschenbach, A. and Nikolov, P. N. (2008). In search of mitochondrial markers for resolving the phylogeny of cyclophyllidea tapeworms (Platyhelminthes, Cestoda) – a test study with Davaineidae. Acta Parasitologica 53, 133–144.CrossRefGoogle Scholar
Loos-Frank, B. (1980 a). The common vole, Microtus arvalis Pall. as intermediate host of Mesocestoides (Cestoda) in Germany. Zeitschrift für Parasitenkunde 63, 129–136.Google ScholarPubMed
Loos-Frank, B. (1980 b). Mesocestoides leptothylacus n. sp. und das nomenklatorische Problem in der Gattung Mesocestoides Vaillant, 1863 (Cestoda, Mesocestoididae). Tropenmedizin und Parasitologie 31, 2–14.Google Scholar
Loos-Frank, B. (1987). Shedding of gravid proglottids and destrobilation in experimental infections of foxes with Mesocestoides leptothylacus Loos-Frank, 1980 (Cestoda). Journal of Helminthology 61, 213–218.CrossRefGoogle ScholarPubMed
Loos-Frank, B. and Zeyhle, E. (1982). The intestinal helminths of the red fox and some other carnivores in southwest Germany. Zeitschrift für Parasitenkunde 67, 99–113.CrossRefGoogle ScholarPubMed
Maddison, D. R. and Madison, W. P. (2000). MacClade 4: Analysis of Phylogeny and Character Evolution, ver. 4. Sinauer Associates, Sunderland, MA, USA.Google Scholar
McAllister, C. T., Bruce Conn, D., Freed, P. S. and Burdick, D. A. (1991). A new host and locality record for Mesocestoides sp. tetrathyridia (Cestoidea: Cyclophyllidea), with a summary of the genus from snakes of the world. The Journal of Parasitology 77, 329–331.CrossRefGoogle ScholarPubMed
McGinnis, S. and Madden, T. L. (2004). BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Research 32, W20–W25.CrossRefGoogle ScholarPubMed
Millán, J., Gortazar, C. and Casanova, J. C. (2003). First occurrence of Mesocestoides sp. in a bird, the red-legged partridge, Alectoris rufa, in Spain. Parasitology Research 90, 80–81.CrossRefGoogle Scholar
Miterpáková, M., Dubinský, P., Reiterová, K., Machková, N., Várady, M. and Šnábel, V. (2003). Spatial and temporal analysis of the Echinococcus multilocularis occurrence in the Slovak Republic. Helminthologia 40, 217–226.Google Scholar
Miterpáková, M., Dubinský, P., Reiterová, K. and Stanko, M. (2006). Climate and environmental factors influencing Echinococcus multilocularis occurence in the Slovak Republic. Annales Agricultural Environmental Medicine 13, 235–242.Google Scholar
Miterpáková, M., Hurníková, Z., Antolová, D. and Dubinský, P. (2009). Endoparasites of red fox (Vulpes vulpes) in the Slovak Republic with the emphasis on zoonotic species Echinococcus multilocularis and Trichinella spp. Helminthologia 46, 73–79.CrossRefGoogle Scholar
Nakao, M., Sako, Y., Yokoyama, N., Fukunaga, M. and Ito, A. (2000). Mitochondrial genetic code in cestodes. Molecular and Biochemical Parasitology 111, 415–424.CrossRefGoogle ScholarPubMed
Nickisch-Rosenegk, M., Lucius, R. and Loos-Frank, B. (1999). Contributions to the phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. Journal of Molecular Evolution 48, 586–596.CrossRefGoogle Scholar
Nylander, J. A. A. (2004). MrModelTest v2. Program disributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden.Google Scholar
Okulewicz, A., Hildebrand, J., Okulewicz, J. and Perec, A. (2005). Red fox (Vulpes vulpes) as reservoir of parasites and source of zoonosis. Wiadomosti Parazytologickije 51, 125–132.Google ScholarPubMed
Olson, P. D. and Tkach, V. V. (2005). Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Advances in Parasitology 58, 165–243.CrossRefGoogle Scholar
Olson, P. D., Littlewood, D. T. J., Bray, R. A. and Mariaux, J. (2001). Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 18, 443–467.CrossRefGoogle Scholar
Olson, P. D., Poddubnaya, L. G., Littlewood, D. T. J. and Scholz, T. (2008). On the position of Archigetes and the early evolution of the tapeworms. The Journal of Parasitology 94, 898–904.CrossRefGoogle ScholarPubMed
Padgett, K. A. and Boyce, W. M. (2004). Life-history studies on two molecular strains of Mesocestoides (Cestoda: Mesocestoididae): identification of sylvatic hosts and infectivity of immature life stages. The Journal of Parasitology 90, 108–113.CrossRefGoogle ScholarPubMed
Padgett, K. A., Nadler, S. A., Munson, L., Sacks, B. and Boyce, W. M. (2005). Systematics of Mesocestoides (Cestoda: Mesocestoididae): evaluation of molecular and morphological variation among isolates. The Journal of Parasitology 91, 1435–1443.CrossRefGoogle ScholarPubMed
Pétavy, A. F., Deblock, S. and Prost, C. (1990). Epidemiology of alveolar echinococcosis in France.1.Intestinal helminths in the red fox (Vulpes vulpes L.) from Haute-Savoie. Annales de Parasitologie Humaine et Comparée 65, 22–27.CrossRefGoogle ScholarPubMed
Pleijel, F., Jondelius, U., Norlinder, E., Nygren, A., Oxelman, B., Schander, C., Sundberg, P. and Thollesson, M. (2008). Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Priemer, E. (1983). On the problem of European Mesocestoides species (Cestoda) from mammals. Helminthologia 20, 89–95.Google Scholar
Rausch, R. L. (1994). Family Mesocestoididae Fuhrmann, 1907. In Keys to the Cestode Parasites of Vertebrates (ed. Khalil, L. F., Jones, A. and Bray, R. A.), pp. 309–314. CAB International, Wallingford, UK.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Skrjabin, K. I. (1978). Tetrabotrididae and Mesocestoididae – platyhelminths of birds and mammals (in Russian). In Osnovy Cestodologii, part 9 (ed. Skrjabin, K. I.), pp. 156–215. Public House ‘Moskva’, Russia.Google Scholar
Specht, D. and Voge, M. (1965). Asexual multiplication of Mesocestoides tetrathyridia in laboratory animals. The Journal of Parasitology 51, 268–272.CrossRefGoogle ScholarPubMed
Švrček, Š., Zavadová, J., Maďar, M., Ondrejka, R., Suliová, J., Beníšek, Z., Ondrejková, A. and Franka, R. (2000). Recent results of research and development achieved at the Joint Rabiologic Laboratory of the Research Institute of Veterinary Medicine and the University of Veterinary Medicine in Košice. Slovak Veterinary Journal 25, 294–296.Google Scholar
Swofford, D. L. (2003). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), ver. 4.1b. Sinauer Associates, Sunderland, MA, USA.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.CrossRefGoogle Scholar
Thiess, A., Schuster, R., Nöckler, K. and Mix, H. (2001). Helminth findings in indigenous racoon dog Nyctereutes procyonoides (Gray, 1843). Berliner und Münchener tierärztliche Wochenschrift 114, 273–276.Google ScholarPubMed
Toplu, N., Yildiz, K. and Tunay, R. (2004). Massive cystic tetrathyridiosis in a dog. Journal of Small Animal Practice 45, 410–412.CrossRefGoogle Scholar
Voge, M. (1955). North American cestodes of the genus Mesocestoides. University of California Publication in Zoölogy 59, 125–156.Google Scholar
Waeschenbach, A., Webster, B. L., Bray, R. A. and Littlewood, D. T. J. (2007). Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Molecular Phylogenetics and Evolution 45, 311–325.CrossRefGoogle ScholarPubMed
Whelan, S. and Goldman, N. (2001). A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Molecular Biology and Evolution 18, 691–699.CrossRefGoogle ScholarPubMed
WHO/OIE (2001). Manual on Echinococcosis in Humans and Animals: a Public Health Problem of Global Concern (ed. Eckert, J., Gemmell, F.-X., Meslin, Z. and Pawlowski, ). World Organisation of Animal Health, Paris, France.Google Scholar
Willingham, A. L., Ockens, N. W., Kapel, C. M. O. and Monrad, J. (1996). A helminthological survey of wild red foxes (Vulpes vulpes) from the metropolitan area of Copenhagen. Journal of Helminthology 70, 259–263.Google ScholarPubMed
Wirtherle, N., Wiemann, A., Ottenjann, M., Linzmann, H., van der Grinten, E., Kohn, B., Gruber, A. D. and Clausen, P. H. (2007). First case of canine peritoneal larval cestodosis caused by Mesocestoides lineatus in Germany. Parasitology International 56, 317–320.CrossRefGoogle ScholarPubMed