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Occurrence of Mesocestoides canislagopodis (Rudolphi, 1810) (Krabbe, 1865) in mammals and birds in Iceland and its molecular discrimination within the Mesocestoides species complex

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Abstract

The life cycle of Mesocestoides tapeworms (Cestoda: Cyclophyllidea: Mesocestoididae) requires three hosts. The first intermediate host is unknown but believed to be an arthropod. The second intermediate host is a vertebrate. The primary definitive host is a carnivore mammal, or a bird of prey, that eats the tetrathyridium-infected second intermediate host. One representative of the genus, Mesocestoides canislagopodis, has been reported from Iceland. It is common in the arctic fox (Vulpes lagopus) and has also been detected in domestic dogs (Canis familiaris) and cats (Felis domestica). Recently, scolices of a non-maturing Mesocestoides sp. have also been detected in gyrfalcon (Falco rusticolus) intestines, and tetrathyridia in the body cavity of rock ptarmigan (Lagopus muta). We examined the taxonomic relationship of Mesocestoides from arctic fox, gyrfalcon, and rock ptarmigan using molecular methods, both at the generic level (D1 domain LSU ribosomal DNA) and at the specific level (cytochrome c oxidase subunit I (COI) and 12S mitochondrial DNA). All stages belonged to Mesocestoides canislagopodis. Phylogenetic analysis of the combined 12S-COI at the specific level confirmed that M. canislagopodis forms a distinct clade, well separated from three other recognized representatives of the genus, M. litteratus, M. lineatus, and M. corti/vogae. This is the first molecular description of this species. The rock ptarmigan is a new second intermediate host record, and the gyrfalcon a new primary definitive host record. However, the adult stage seemed not to be able to mature in the gyrfalcon, and successful development is probably restricted to mammalian hosts.

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References

  • Al-Sabi MN, Chriél M, Jensen TH, Enemark HL (2013) Endoparasites of the raccoon dog (Nyctereutes procyonoides) and the red fox (Vulpes vulpes) in Denmark 2009–2012—a comparative study. Int J Parasitol Parasites Wildl 2:144–51

    Article  PubMed  PubMed Central  Google Scholar 

  • Al-Sabi MN, Halasa T, Kapel CM (2014) Infections with cardiopulmonary and intestinal helminths and sarcoptic mange in red foxes from two different localities in Denmark. Acta Parasitol 59:98–107

    Article  PubMed  Google Scholar 

  • Baer JG (1962) Cestoda. The Zoology of Iceland. Vol. 2 (12). Ejnar Munksgaard, Copenhagen and Reykjavik, 63 pp

  • Bowles J, McManus DP (1994) Genetic characterization of the Asian Taenia, a newly described taeniid cestode of humans. Am J Trop Med Hyg 50:33–44

    CAS  PubMed  Google Scholar 

  • Bowles J, Blair D, McManus DP (1995) A molecular phylogeny of the human schistosomes. Mol Phylogenet Evol 4:103–9

    Article  CAS  PubMed  Google Scholar 

  • Braestrup FW (1941) A Study on the arctic fox in Greenland. Immigrations, fluctuations in numbers based mainly on trading statistics. Meddelelser om Grönland. Bd. 131. C.A. Reitzels Forlag. København

  • Chandler AC (1949) Introduction to parasitology. John Wiley and Sons, New York

    Google Scholar 

  • Chertkova AN, Kosupko GA (1978) The suborder Mesocestoidata Skryabin, 1940. In: Ryzhikov KM (ed) Principles of Cestodology. Nauka, Moscow, pp 118–229 [In Russian]

    Google Scholar 

  • Christensen ND, Skirnisson K, Nielsen OK (2015) The parasite fauna of the gyrfalcon (Falco rusticolus) in Iceland. J Wildl Dis 51:929–33

    Article  CAS  PubMed  Google Scholar 

  • Cho SH, Kim TS, Kong Y, Na BK, Sohn WM (2013) Tetrathyridia of Mesocestoides lineatus in Chinese snakes and their adults recovered from experimental animals. Korean J Parasitol 51:531–6

    Article  PubMed  PubMed Central  Google Scholar 

  • Clausen B, Gudmundsson F (1981) Causes of mortality among free-ranging gyrfalcons in Iceland. J Wildl Dis 17:105–9

    Article  CAS  PubMed  Google Scholar 

  • Conn DB (1990) The rarity of asexual reproduction among Mesocestoides tetrathyridia (Cestoda). J Parasitol 76:453–5

    Article  CAS  PubMed  Google Scholar 

  • Conn DB, Galán-Puchades MT, Fuentes MV (2010) Interactions between anomalous excretory and tegumental epithelia in aberrant Mesocestoides tetrathyridia from Apodemus sylvaticus in Spain. Parasitol Res 106:1109–15

    Article  PubMed  Google Scholar 

  • Conn DB, Galán-Puchades MT, Fuentes MV (2011) Normal and aberrant Mesocestoides tetrathyridia from Crocidura spp. (Soricimorpha) in Corsica and Spain. J Parasitol 97:915–9

    Article  PubMed  Google Scholar 

  • Dinkel A, Kern S, Brinker A, Oehme R, Vaniscotte A, Giraudoux P, Mackenstedt U, Romig T (2011) A real-time multiplex-nested PCR system for coprological diagnosis of Echinococcus multilocularis and host species. Parasitol Res 109:493–8

    Article  PubMed  Google Scholar 

  • Eira C, Torres J, Vingda J, Miquel J (2006) Ecological aspects influencing the helminth community of the wood mouse Apodemus sylvaticus in Dunas de Mira, Portugal. Acta Parasitol 51:300–8

    Google Scholar 

  • Eleni C, Scaramozzino P, Busi M, Ingrosso S, D’Amelio S, De Liberato C (2007) Proliferative peritoneal and pleural cestodiasis in a cat caused by metacestodes of Mesocestoides sp. Anatomohistopathological findings and genetic identification. Parasite 14:71–6

    Article  CAS  PubMed  Google Scholar 

  • Etges FJ (1991) The proliferative tetrathyridium of Mesocestoides vogae sp. n. (Cestoda). J Helminthol Soc Wash 58:181–5

    Google Scholar 

  • Foronda P, Perez Rivero A, Santana Morales MA, Kabdur A, Gonzalez AC, Quispe Ricalde MA, Feliu C, Valladares B (2007) First larval record of Mesocestoides in carnivora of Tenerife (Canary Islands). J Parasitol 93:138–42

    Article  CAS  PubMed  Google Scholar 

  • Gallas M, Silveira EF (2011) Mesocestoides sp. (Eucestoda, Mesocestoididae) parasitizing four species of wild felines in Southern Brazil. Rev Bras Parasitol Vet 20:168–70

    Article  PubMed  Google Scholar 

  • Gubány A, Eszterbauer E (1998) Morphological investigation of Mesocestoides (Cestoda, Mesocestoididae) species parasitizing Vulpes vulpes in Hungary. Miscellanea Zoologica Hungarica 12:11–9

    Google Scholar 

  • Guðmundsson F (1972) Grit as an indicator of the overseas origin of certain birds occurring in Iceland. IBIS 114:582

    Google Scholar 

  • Goüy de Bellocq J, Sarà M, Casanova JS, Feliu C, Morand S (2003) A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitol Res 90:64–70

    Google Scholar 

  • Hersteinsson P (1993) Tófan [The Arctic fox]. In: Hersteinsson P, Sigbjarnarson G (eds) Villt, íslensk spendýr. HÍN and Landvernd, Reykjavík, pp 15–48 [In Icelandic]

    Google Scholar 

  • Hoeppli RJC (1925) Mesocestoides corti, a new species of cestode from the mouse. J Parasitol 12:91–6

    Article  Google Scholar 

  • Hrčkova G, Miterpakova M, O’Connor A, Snabel V, Olson PD (2011) Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe. Parasitology 138:638–47

    Article  PubMed  Google Scholar 

  • Jabbar A, Papini R, Ferrini N, Gasser RB (2012) Use of a molecular approach for the definitive diagnosis of proliferative larval mesocestoidiasis in a cat. Infect Genet Evol 12:1377–80

    Article  PubMed  Google Scholar 

  • Kapel CM, Nansen P (1996) Gastrointestinal helminths of Arctic foxes (Alopex lagopus) from different bioclimatological regions in Greenland. J Parasitol 82:17–24

    Article  CAS  PubMed  Google Scholar 

  • Krabbe H (1865) Helminthologiske undersøgelser i Denmark og paa Island med særlige hensyn til blæreormelidelser paa Island. Kongelige Danske Videnskabernes Selskabs Skrifter, 5. Række, naturvidensk. og mathem. afdeling, 7. Bind, 71pp [In Danish]

  • Lee SU, Huh S, Sohn WM, Chai JY (2004) Sequence comparisons of 28S ribosomal DNA and mitochondrial cytochrome c oxidase subunit I of Metagonimus yokogawai, M. takahashii and M. miyatai. Korean J Parasitol 42:129–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Literák I, Olson PD, Georgiev BB, Spakulova M (2004) First record of metacestodes of Mesocestoides sp. in the common starling (Sturnus vulgaris) in Europe, with and 18S rDNA characterization of the isolate. Folia Parasitol 51:45–9

    Article  PubMed  Google Scholar 

  • Literák I, Tenora F, Letkova V, Goldova M, Torres J, Olson PD (2006) Mesocestoides litteratus (Batsch, 1786) (Cestoda: Cyclophyllidea: Mesocestoididae) from the red fox: morphological and 18S rDNA characterization of European isolates. Helminthologia 43:191–5

    Article  Google Scholar 

  • Littlewood DTJ, Rohde K, Bray RA, Herniou EA (1999) Phylogeny of the Platyhelminthes and the evolution of parasitism. Biol J Linn Soc 68:257–87

    Article  Google Scholar 

  • Littlewood DTJ, Waeschenbach A, Nikolov PN (2008) In search of mitochondrial markers for resolving the phylogeny of cyclophyllidean tapeworms (Platyhelminthes, Cestoda)—a test study with Davaineidae. Acta Parasitol 53:133–44

    Article  CAS  Google Scholar 

  • Loos-Frank B (1980) Mesocestoides leptothylacus n. sp.und das nomenklaturische Problem in der Gattung Mesocestoides Vaillant, 1863 (Cestoda, Mesocestoididae). Tropenmedizin und Parasitologie 31:1–14 [In German]

    Google Scholar 

  • Loos-Frank B (1987) Shedding of gravid proglottids and destrobilation in experimental infections of foxes with Mesocestoides leptothylacus Loos-Frank, 1980 (Cestoda). J Helminthol 61:213–18

    Article  CAS  PubMed  Google Scholar 

  • Loos-Frank B (1991) One or two intermediate hosts in the life cycle of Mesocestoides (Cyclophyllidea, Mesocestoididae)? Parasitol Res 77:726–28

    Article  CAS  PubMed  Google Scholar 

  • Loos-Frank B, Skirnisson K, Eydal M (1992) Mesocestoides canislagopodis (Rudolphi, 1810) (Krabbe, 1865) (Cestoda: Mesocestoididae) from arctic foxes, Alopex lagopus (L.) in Iceland redescribed. Bull Scand Soc Parasitol 2:68–73

    Google Scholar 

  • Manios N, Papazahariadou M, Frydas S, Papageorgiou N, Tsachalidis E, Georgopoulou J (2002) Tetrathyridium as a mortality factor of rock partridge (Alcetoris graeca gracea) in Central Greece. Z Jagdwiss 48:378–82

    Google Scholar 

  • McAllister CT, Conn DB (1990) Occurrence of Mesocestoides sp. tetrathyridia (Cestoidea: Cyclophyllidea) in North American anurans (Amphibia). J Wildl Dis 26:540–43

    Article  CAS  PubMed  Google Scholar 

  • Meijer T, Mattson R, Angerbjörn A, Osterman-Lind E, Fernández-Aguilar X, Gavier-Widén D (2011) Endoparasites in the endangered Fennoscandian population of arctic foxes (Vulpes lagopus). Eur J Wildl Res 57:923–7

    Article  Google Scholar 

  • Millán J, Gortazar C, Casanova JC (2003) First occurrence of Mesocestoides sp. in a bird, the red-legged partridge, Alectoris rufa, in Spain. Parasitol Res 90:80–1

    PubMed  Google Scholar 

  • Nakao M, Sako Y, Yokoyama N, Fukunaga M, Ito A (2000) Mitochondrial genetic code in cestodes. Mol Biochem Parasitol 111:415–24

    Article  CAS  PubMed  Google Scholar 

  • Nickisch-Rosenegk M, Richard L, Loos-Frank B (1999) Contributions to the phylogeny of the Cyclophyllidea (Cestoda) inferred from mitochondrial 12S rDNA. J Mol Evol 48:586–96

    Article  Google Scholar 

  • Ólafsson E (1991) Íslenskt skordýratal [Insects of Icleland]. Fjölrit Náttúrufræðistofnunar 17:1–69 [In Icelandic]

    Google Scholar 

  • Olson PD, Littlewood DT, Bray RA, Mariaux J (2001) Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol Phylogenet Evol 19:443–67

    Article  CAS  PubMed  Google Scholar 

  • Padgett KA, Boyce WM (2004) Life-history studies on two molecular strains of Mesocestoides (Cestoda: Mesocestoididae): identification of sylvatic hosts and infectivity of immature life stages. J Parasitol 90:108–13

    Article  PubMed  Google Scholar 

  • Padgett KA, Boyce WM (2005) Ants as first intermediate hosts of Mesocestoides on San Miguel Island, USA. J Helminthol 79:67–73

    Article  CAS  PubMed  Google Scholar 

  • Padgett KA, Nadler SA, Munson L, Sacks B, Boyce WM (2005) Systematics of Mesocestoides (Cestoda: Mesocestoididae): evaluation of molecular and morphological variation among isolates. J Parasitol 91:1435–43

    Article  CAS  PubMed  Google Scholar 

  • Padgett KA, Crosbie PR, Boyce WM (2013) Mesocestoides. In: Liu D (ed) Molecular detection of human pathogens. CRC Press, Taylor and Francis Group, pp 277–85

    Google Scholar 

  • Rausch RL (1994) Family Mesocestoididae Fuhrmann, 1907. In: Khalil LF, Jones A, Bray RA (eds) Keys to the cestode parasites of vertebrates. CAB International, Wallingford, pp 309–14

    Google Scholar 

  • Saeed I, Maddox-Hyttel C, Monrad J, Kapel CM (2006) Helminths of red foxes (Vulpes vulpes) in Denmark. Vet Parasitol 139:168–79

    Article  CAS  PubMed  Google Scholar 

  • Sato H, Ihama Y, Inaba T, Yagisawa M, Kamiya H (1999) Helminth fauna of carnivores distributed in north-western Tohoku, Japan, with special reference to Mesocestoides paucitesticulus and Brachylaima tokudai. J Vet Med Sci 61:1339–42

    Article  CAS  PubMed  Google Scholar 

  • Shults LM (1970) Mesocestoides kirby and M. lineatus: occurrence in Alaskan carnivores. Trans Am Microsc Soc 89:478–86

    Article  Google Scholar 

  • Skirnisson K, Eydal M, Gunnarsson E, Hersteinsson P (1993) Parasites of the arctic fox Alopex lagopus in Iceland. J Wildl Dis 29:440–46

    Article  CAS  PubMed  Google Scholar 

  • Skirnisson K, Richter SH, Eydal M (2003) Prevalence of human parasites in Iceland: past and present status. In: Akkuffo H, Ljungström I, Linder E, Whalgren M (eds) Parasites of the colder climates. Taylor and Francis, London and New York, pp 34–44

    Google Scholar 

  • Skirnisson K, Sigurðardóttir ÓG, Nielsen ÓK. Morphological characteristics of Mesocestoides canislagopodis (Krabbe 1865) tetrathyridia found in rock ptarmigan Lagopus muta in Iceland. Parasitol Res (in press)

  • Stien A, Irvine RJ, Ropstad E, Halvorsent O, Langvatn R, Albon SD (2002) The impact of gastrointestinal nematodes on wild reindeer: experimental and cross-sectional studies. J Anim Ecol 71:937–45

    Article  Google Scholar 

  • Stien A, Voutilainen L, Haukisalmi V, Fuglei E, Mørk T, Yoccoz NG, Ims RA, Henttonen H (2010) Intestinal parasites of the Arctic fox in relation to the abundance and distribution of intermediate hosts. Parasitology 137:149–57

    Article  CAS  PubMed  Google Scholar 

  • Soldatova AP (1944) A contribution to the study of the development cycle in cestoda Mesocestoides lineatus (Goeze, 1782), parasitic of carnivorous mammals. Dokl Akad Nauk USSR 45:310–12

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tokiwa T, Taira K, Yamazaki M, Kashimura A, Une Y (2014) The first report of peritoneal tetrathyridiosis in squirrel monkey (Saimiri sciureus). Parasitol Int 63:705–7

    Article  PubMed  Google Scholar 

  • Vaillant L (1863) Sur deux helminthes cestoïde de la Genette. Inst, Paris, 1er Sect, Sc Math. Phys Nat 31:87–8

    Google Scholar 

  • Voge M (1967) Development in vitro of Mesocestoides (Cestoda) from oncosphere to young tetrathyridium. J Parasitol 53:78–82

    Article  CAS  PubMed  Google Scholar 

  • Voge M, Seidel JS (1968) Continuous growth in vitro of Mesocestoides (Cestoda) from oncosphere to fully developed tetrathyridium. J Parasitol 54:269–71

    Article  CAS  PubMed  Google Scholar 

  • Waeschenbach A, Webster BL, Bray RA, Littlewood DT (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–25

    Article  CAS  PubMed  Google Scholar 

  • Wirtherle N, Wiemann A, Ottenjann M, Linzmann H, van der Grinten E, Kohn B, Gruber AD, Clausen PH (2007) First case of canine peritoneal larval cestodosis caused by Mesocestoides lineatus in Germany. Parasitol Int 56:317–20

    Article  CAS  PubMed  Google Scholar 

  • Yamaguti S (1959) Systhema helminthum: the cestodes of vertebrates. Interscience Publishers Inc., New York

    Google Scholar 

  • Yanchev Y (1986) On the morphology, taxonomy and distribution of the species of the genus Mesocestoides Vailland, 1863 in Bulgaria. Khelmintologiya 21:45–65 [In Bulgarian]

    Google Scholar 

  • Zalesny G, Hildebrand J (2012) Molecular identification of Mesocestoides spp. from intermediate hosts (rodents) in central Europe (Poland). Parasitol Res 110:1055–61

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Johann Evensen for providing the arctic fox for analysis. Nanna Daugbjerg Christensen helped with examining gyrfalcon parasites, and in the past 10 years more than 40 persons have assisted in the field and in the laboratory in sampling and examining rock ptarmigan. Bruce Conn commented on an early draft of the manuscript. Financial support was provided by the Research Fund of the University of Iceland and the Icelandic Research Fund (grant number 090207021), and the Icelandic Institute of Natural History. In France, financial support was provided by the PHC Jules Verne Program for French–Icelandic scientific cooperation and Office National de la Chasse et de la Faune Sauvage (ONCFS).

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  1. Laboratory of Parasitology, Institute for Experimental Pathology, University of Iceland, Keldur, IS-112, Reykjavík, Iceland

    Karl Skirnisson

  2. EA4688 « Vecpar », UFR de Pharmacie, Université de Reims Champagne-Ardenne, 51 rue Cognacq-Jay, 51096, Reims Cedex, France

    Damien Jouet & Hubert Ferté

  3. Icelandic Institute of Natural History, Urriðaholtsstræti 6-8, 210, Garðabær, Iceland

    Ólafur K. Nielsen

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  1. Karl Skirnisson
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Correspondence to Karl Skirnisson.

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Skirnisson, K., Jouet, D., Ferté, H. et al. Occurrence of Mesocestoides canislagopodis (Rudolphi, 1810) (Krabbe, 1865) in mammals and birds in Iceland and its molecular discrimination within the Mesocestoides species complex. Parasitol Res 115, 2597–2607 (2016). https://doi.org/10.1007/s00436-016-5006-5

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