Rodents as intermediate hosts of cestode parasites of mammalian carnivores and birds of prey in Poland, with the first data on the life-cycle of Mesocestoides melesi

Abstract

Background: Rodents constitute an important part of the diet of many carnivore species. This predator-prey food chain is exploited by helminth parasites, such as cestodes, whose larval stages develop in rodents and then mature to the adult stage in predators. The main aim of our study was to use molecular techniques for identification of cestode species recovered from both intermediate and definitive hosts, with a particular focus on the genus Mesocestoides.

Methods: Larval cestodes were obtained during our long-term studies on rodent helminth communities in the Mazury Lake District in the north-east Poland in 2000-2018. Cestode larvae/cysts were collected from body cavities or internal organs (e.g. liver) during autopsies. Adult tapeworms were derived from nine red foxes, three Eurasian badgers and one Eurasian lynx. PCR amplification, sequencing and phylogenetic analyses were conducted employing three genetic markers: 18S rDNA, mitochondrial (mt) 12S rDNA and the mt cytochrome c oxydase subunit 1 (cox1) gene fragment.

Results: Altogether 19 Mesocestoides samples were analyzed, including 13 adult tapeworms from definitive hosts and six larval samples from 4 bank voles and 2 yellow-necked mice. Phylogenetic analyses revealed three well-supported trees of similar topology. In each case the Mesocestoides samples formed two separate clades. All isolates from foxes, the lynx isolate and two isolates from rodents grouped with Mesocestoides litteratus. Four isolates from rodents and all three isolates from Eurasian badgers were resolved in a separate clade, most similar to North American M. vogae (syn. M. corti). Examination of fixed, stained adult specimens from Eurasian badgers revealed consistency with the morphology of Mesocestoides melesi. Therefore, this clade is likely to represent M. melesi, a species first described in 1985 from the Eurasian badger Meles meles. Molecular analysis allowed also the identification of Taenia crassiceps, Hydatigera kamiyai and Cladotaenia globifera among larvae derived from rodents.

Conclusions: Molecular and phylogenetic analyses support the recognition of M. melesi as a valid species. Our data represent the first record of the larvae of this species in rodents. This is the first report on the occurrence of H. kamiyai in rodents from Poland.

Keywords: Badger; Fox; Hydatigera; Lynx; Mesocestoides; Rodents; Taenia crassiceps.

Fig. 1

Maximum likelihood tree for Mesocestoides and relatives based on 18S rDNA (GTR + G model). Numbers along branches are bootstrap support (BS) and posterior probability (PP) values if corresponding bipartition was found in Bayesian 50% majority rule consensus tree. Only values of BS higher than 75% and PP higher than 0.95 are shown. The scale-bar indicates the expected number of nucleotide substitutions per site

Fig. 2

Maximum likelihood tree for Mesocestoides and relatives based on mt 12S rDNA (GTR + G model). Numbers along branches are bootstrap support (BS) and posterior probability (PP) values if corresponding bipartition was found in Bayesian 50% majority rule consensus tree. Only values of BS higher than 75% and PP higher than 0.95 are shown. The scale-bar indicates the expected number of nucleotide substitutions per site

Fig. 3

Maximum likelihood tree for Mesocestoides and relatives based on cox1 gene fragment (GTR + G model). Numbers along branches are bootstrap support (BS) and posterior probability (PP) values if corresponding bipartition was found in Bayesian 50% majority rule consensus tree. Only values of BS higher than 75% and PP higher than 0.95 are shown. The scale-bar indicates the expected number of nucleotide substitutions per site