Intermediate hosts of the trematode Collyriclum faba (Plagiochiida: Collyriclidae) identified by an integrated morphological and genetic approach

Abstract

Background

The cutaneous monostome trematode Collyriclum faba (Bremser in Schmalz, 1831) is a bird parasite with a hitherto unknown life cycle and highly focal occurrence across the Holarctic and Neotropic ecozones.

Methods

Representative specimens of benthic organisms were sampled at multiple sites and dates within the known foci of C. faba occurrence in Slovakia. A combined approach involving detailed morphological examination and sequencing of two independent DNA loci was used for their analysis.

Results

We elucidated the complete life cycle of C. faba, which we determined to include the aquatic gastropod mollusk Bythinella austriaca (Frauenfeld, 1857) as the first intermediate host, the mayflies of the family Heptageniidae, Ecdyonurus venosus (Fabricius, 1775) and Rhithrogena picteti Sowa, 1971 x iridina (Kolenati, 1839), as the second intermediate hosts, and birds (primarily but not exclusively passeriform birds) as the definitive hosts. Bythinella austriaca occurs focally in the springs of tributaries of the Danube in the Alpine-Carpathian region. The restricted distribution of B. austriaca explains the highly focal distribution of C. faba noticed previously in spite of the broad distribution of its second intermediate and definitive host species. Utilization of both larval and adult Ephemeroptera spp. as the second intermediate hosts explains the known spectrum of the definitive host species, with the highest prevalence in species feeding on larvae of Ephemeroptera, such as Cinclus cinclus (Linnaeus, 1758) and Motacilla cinerea Tunstall, 1771, or adults of Ephemeroptera, such as Sylvia atricapilla (Linnaeus, 1758) and Regulus regulus (Linnaeus, 1758). In this study, we also determine the prevalence and DNA sequences of other immature trematode specimens found in the examined benthic organisms (particularly the families Microphallidae, Troglotrematidae and Nanophyetidae and Euryhelmis zelleri Grabda-Kazubska, 1980, Heterophyidae), and describe cercariae of C. faba.

Conclusions

We determined the full life cycle of the Central European populations of C. faba. We speculate that other species of Bythinella and the closely related genus Amnicola may serve as first intermediate hosts in other parts of the distribution range of C. faba. Similarly, other Ephemeroptera of the family Heptageniidae may serve as the second intermediate hosts of C. faba in the Americas.

Electronic supplementary material

The online version of this article (doi:10.1186/s13071-015-0646-3) contains supplementary material, which is available to authorized users.