The Natural Infection of Freshwater Snails with the Avian Air Sac Fluke, Cyclocoelum mutabile (Trematoda: Cyclocoelidae), in Brazil

Trematodes of the family Cyclocoelidae are parasites mainly of the respiratory system of birds and present a cosmopolitan distribution. Although infection with these flukes can result in pathological changes and even bird death, information on their life cycles is scarce and almost entirely based on experimental infection data. Thus, the generation of knowledge on the mollusks that act as natural intermediate hosts of cyclocoelids is necessary and can aid control measures against these air sac trematodes. In the present study, gastropod mollusks collected in an urban stream from Belo Horizonte, Minas Gerais, Brazil, were subjected to the compression technique for the detection of non-emerging larval trematodes. Tailless cercariae with confluent ceca were found in 8/30 (26.7%) specimens of Biomphalaria glabrata and 3/33 (9.1%) specimen of Physella acuta. Samples of the cercariae were subjected to morphological characterization and genetic study (28S, Cox-1, and Nad-1). For comparative purposes, adult trematodes previously collected in the air sac of a common gallinule (Gallinula galeata) found dead in another waterbody from the same region were also characterized. The molecular sequences obtained revealed a high degree of similarity (100% in 28S, 99.2% in Cox-1, and 99.5% in Nad-1) between larval stages found in mollusks and adult parasites found in G. galeata and morphologically identified as Cyclocoelum mutabile. The conspecificity with this widely distributed cyclocoelid was also corroborated by phylogenetic analysis and comparison with isolates of this species previously characterized in Peru and the Czech Republic (99.4–100% and 96.7–97.0% of similarity in Nad-1, respectively). Thus, the integrative analysis carried out in the present work enabled us to identify C. mutabile in mollusks in South America for the first time. The finding of B. glabrata and P. acuta as new intermediate hosts corroborates the importance of freshwater gastropods in the transmission of C. mutabile, as well as the low specificity to the mollusk group, as previously characterized through experimental studies.