Necropsy of two free-ranging common blackbirds (Turdus merula) found dead in central Italy revealed the presence of a high number of cyclocoelid flukes in the coelomatic cavity. Cyclocoelid flukes primarily infect avian respiratory system. Histologically, air sac walls were covered with a fibrinous exudate containing degenerate heterophils, many trematodes and some colonies of Gram-positive cocci. The superficial bronchi and parabronchi were markedly distended, and the adjacent pulmonary parenchyma was congested and collapsed. Trematodes, surrounded by a mild suppurative to pyogranulomatous inflammatory reaction, were also observed on the pericardial, intestinal, kidney and hepatic serosal surfaces. The death of the two examined birds was likely due to the high parasite load and associated severe lesions. At parasitological examination, flukes showed a tongue-shaped elongate body, tapered anteriorly and rounded posteriorly, of 2,088-2,314 μm in width and 8,268-11,830 μm in length. The mouth was slightly oval and sub-terminal, with a small oral sucker. The oval pharynx measured 250-309 μm, and the two caeca joined posteriorly. Two large (550-702 μm × 450-520 μm) globular testes were situated obliquely to each other, whereas an oval (250 × 300 μm in mean) or round (about 334 μm in diameter) intertesticular ovary was placed in a longitudinal straight line with the testes. The ootype was about 110 μm in diameter, while the brown-yellow eggs measured 131.5 × 73.9 μm in mean. The genital pore was post-pharyngeal, while the symmetrically arranged vitelline glands were not confluent posteriorly. Morphoflogical diagnosis led to the identification of Morishitium polonicum, a cyclocoelid fluke species that typically inhabits the air sacs of blackbirds. The morphological diagnosis was corroborated by molecular phylogenetic analysis of the mitochondrial (CO1, ND1) DNA loci. The present study provides the first report of pathological lesions and death caused by M. polonicum in birds.

Charles University 3rd Faculty of Medicine Prague Czech Republic

Comenius Museum Moravian Ornithological Station Přerov Czech Republic

Department of Veterinary Sciences University of Pisa Pisa Italy

School of Biosciences and Veterinary Medicine Matelica University of Camerino Italy

See more in PubMed

BirdLife International . IUCN; 2016. "Turdus merula". The IUCN Red List of Threatened Species. 2016: e.T103888106A87871094. doi:10.2305/IUCN.UK.2016-3.RLTS.T103888106A87871094.en.

Bowles J., Blair D., McManus D.P. Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Mol. Biochem. Parasitol. 1992;54:165–173. PubMed

Branton S.L., Deaton J.W., Gerlach H., Ruff M.D. Cyclocoelum mutabile infection and aortic rupture in an American coot (Fulica americana) Avian Dis. 1985;29:246–249. PubMed

Bray R.A., Littlewood D.T.J., Herniov E.A., Williams B., Henderson R.E. Digenean parasites of deep-sea teleosts: a review and case studies of intrageneric phylogenies. Parasitology. 1999;119:5125–5144. PubMed

Brym M.Z., Henry C., Kendall R.J. Elevated parasite burdens as a potential mechanism affecting northern bobwhite (Colinus virginianus) population dynamics in the Rolling Plains of West Texas. Parasitol. Res. 2018;117:1683–1688. PubMed

Calegaro-Marques C., Amato S.B. Urbanization breaks up host-parasite interactions: a case study on parasite community ecology of Rufous-bellied Thrushes (Turdus rufiventris) along a rural-urban gradient. PLoS One. 2014;9:e103144. PubMed PMC

Cardells J., Ortega J., Martinez-Herrero M.C., Martischarfhausen M.R., Villamayor M., Dominguez V., Pereira P., Catalagregori P., Severino R., Garijo M. Proceedings of the 51 Congreso Científico de Avicultura (Valencia) 2-3 October 2014. 2014. Influencia del estado parasitario de los tordos (Turdus spp.) sobre su condición corporal.http://www.wpsa-aeca.es/articulo.php?id_articulo=3724

Ching H.L. Helminths of varied thrushes, Ixoreus naevius and robins Turdus migratorius, from British Columbia. Proc. Helminthol. Soc. Wash. 1993;60:239–242.

Clement P., Hathway R., Wilczur J. Christopher Helm Publishers Ltd.; London, UK: 2000. Thrushes (Helm Identification Guides)

Cole R.A., Thomas N.J., Roderick C.L. Bothrigaster vanolans (Trematoda: Cyclocoelidae) infection in two Florida snail kites (Rostrhamus sociabilis plumbeus) J. Wildl. Dis. 1995;31:576–578. PubMed

Delaski K.M., Nelson S., Dronen N.O., Craig T.M., Pond J., Gamble K.C. Detection and management of air sac trematodes (Szidatitrema species) in captive multispecies avian exhibits. J. Avian Med. Surg. 2015;29:345–353. PubMed

Dronen N.O., Craig T.M., Hammond E.E. Szidatitrema yamagutii n. sp. (Digenea: Cyclocoelidae: Ophthalmophaginae) from the bearded barbet, Lybius dubius (Capitionidae), and the white-necked myna, Streptocitta albicollis (Sturnidae), that died at the Audubon Zoo in New Orleans, Louisiana, U.S.A. Zootaxa. 2006;1219:59–68.

Dronen N.O. Revision of the family Cyclocoelidae Stossich, 1902 with the proposal of two new subfamilies and the description of a new species of Morishitium Witenberg, 1928 from the common snipe, Gallinago gallinago, from Texas, U.S.A. Zootaxa. 2007;1563:55–68.

Dronen N.O., Greiner E.C., Ialeggio D.M., Nolan T.S. Circumvitellatrema momota n. gen., n. sp. (Digenea: Cyclocoelidae: Cyclocoelinae) from a captive-hatched blue-crowned motmot, Momotus momota (Momotidae) Zootaxa. 2009;2161:60–68.

Dronen N.O., Blend C.K. Updated keys to the genera in the subfamilies of Cyclocoelidae Stossich, 1902, including a reconsideration of species assignments, species keys and the proposal of a new genus in Szidatitreminae Dronen, 2007. Zootaxa. 2015;4053:1–100. PubMed

Granroth-Wilding H.M., Daunt F., Cunningham E.J., Burthe S.J. Between-individual variation in nematode burden among juveniles in a wild host. Parasitology. 2017;144:248–258. PubMed

Grünberg W., Kutzer E. Die Pathologie verschiedener Trematodeninfektionen bei Störchen (Ciconia ciconia L., Ciconia nigra L.) Zentralblatt für Veterinarmed. 1964;11B:712–727.

Hamer G.L., Muzzall P.M. Helminths of American robins, Turdus migratorius, and house sparrows, Passer domesticus (order: Passeriformes), from suburban Chicago, Illinois, USA. Comp. Parasitol. 2013;80:287–291.

Hamilton W.D., Zuk M. Heritable true fitness and bright birds: a role for parasites? Science. 1982;218:384–387. PubMed

Hawley D.M., Altizer S.M. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct. Ecol. 2011;25:48–60.

Höfle U., Krone O., Blanco J.M., Pizarro M. Chaunocephalus ferox in free-living white storks in Central Spain. Avian Dis. 2003;47:506–512. PubMed

Hudson P.J., Dobson A.P., Newborn D. Prevention of population cycles by parasite removal. Science. 1998;282:2256–2258. PubMed

Jaume-Ramis S., Pinya S. First record of Morishitium polonicum (Machalska, 1980) (Trematoda, Cyclocoelidae) parasitizing Turdus philomelos Brehm, 1831 in Mallorca (Balearic Islands, Spain) Boll. Soc. Hist. Nat. Balears. 2018;61:9–15.

Leung T.L., Koprivnikar J. Nematode parasite diversity in birds: the role of host ecology, life history and migration. J. Anim. Ecol. 2016;85:1471–1480. PubMed

Libert C., Jouet D., Ferté H., Lemberger K., Keck N. Air sac fluke Circumvitellatrema momota in a captive blue-crowned motmot (Momotus momota) in France. J. Zoo Wildl. Med. 2012;43:689–692. PubMed

Liptovszky M., Majoros G., Perge E. Cathaemasia hians in a Black Stork (Ciconia nigra) in Hungary. J. Wildl. Dis. 2012;48:809–811. PubMed

Literák I., Sitko J. Where in Europe should we look for sources of the cutaneous trematode Collyriclum faba infections in migrating birds? J. Helminthol. 2006;80:349–355. PubMed

Loye J.E., Zuk M. Oxford University Press; Oxford: 1991. Bird-parasite Interactions. Oxford Ornithology Series.

Machalska J. Cyclocoelum polonicum sp. n. (Trematoda, Cyclocoelidae) from the thrushes Turdus philomelos Br. and T. merula L. Acta Parasitol. Pol. 1980;26:129–136.

Mani P., Rossi G., Perrucci S., Bertini S. Mortalità dei merli (Turdus merula) in Toscana. Selezione Veterinaria. 1998;8:749–753.

Martínez F., Hernández S., Calero R., Becerra C., Moreno T., Domínguez de Tena M., Acosta M.I. Parásitos de aves paseriformes en la Provincia de Córdoba. Rev. Iber. Parasitol. 1977;37:133–141.

McDonald J.L., Robertson A., Silk M.J. Wildlife disease ecology from the individual to the population: insights from a long‐term study of a naturally infected European badger population. J. Anim. Ecol. 2018;87:101–112. PubMed

Møller A.P., Allander K., Dufva R. Fitness effects of parasites on passerine birds: a review. In: Blondel J., Gosler A., Lebreton J.D., McCleery R., editors. Population Biology of Passerine Birds. Springer; Berlin, Heidelberg: 1990. pp. 269–280.

Morgan J.A., Blair D. Mitochondrial ND1 gene sequences used to identify echinostome isolates from Australia and New Zealand. Int. J. Parasitol. 1998;28:493–502. PubMed

Moudgil A.D., Singla L.D. Role of neglected wildlife disease ecology in emergence and resurgence of parasitic diseases. Trends Parasitol. Res. 2013;2:18–23.

Norte A.C., Araujo P.M., Sampaio H.L., Sousa J.P., Ramos J.A. Haematozoa infections in a Great Tit Parus major population in Central Portugal: relationships with breeding effort and health. Ibis. 2009;151:677–688.

Okulewicz A., Sitko J. Parasitic helminthes – probable cause of death of birds. Helminthologia. 2012;49:241–246.

Okulewicz A., Okulewicz J., Sitko J., Wesołowska M. New records of digenean flukes (Trematoda) in birds in Poland. Wiad. Parazytol. 2010;56:67–70. PubMed

Perrucci S., Rossi G., Marconcini A., Mani P. Acantocefali del merlo (Turdus merula) Selezione Veterinaria. 1997;8:827–882.

Sitko J., Bizos J., Heneberg P. Central European parasitic flatworms of the Cyclocoelidae Stossich, 1902 (Trematoda: Plagiorchiida): molecular and comparative morphological analysis suggests the reclassification of Cyclocoelum obscurum (Leidy, 1887) into the Harrahium Witenberg, 1926. Parasitology. 2017;144:368–383. PubMed

Sitko J., Zaleśny G. The effect of urbanization on helminth communities in the Eurasian blackbird (Turdus merula L.) from the eastern part of the Czech Republic. J. Helminthol. 2014;88:97–104. PubMed

Slater R.L. Helminths of the robin, Turdus migratorius Ridgway, from Northern Colorado. Am. Midl. Nat. 1967;77:190–199.

Snow D.W. London British Museum of Natural History; London, UK: 1988. A Study of Blackbirds.

Sulgostowska T., Czaplinska D. Panstwowe Wydawnictwo Naukowe; Wroclaw: 1987. Pasozyty ptakow? Parasiti avium. Zeszyt 1. Pierwotniaki i Przywry. Protozoa et Trematoda. Katalog Fauny Pasozytniczej Polski; p. 210.

Thompson R.C.A., Lymbery A.J., Smith A. Parasites, emerging disease and wildlife conservation. Int. J. Parasitol. 2010;40:1163–1170. PubMed

Thompson R.C.A. Parasite zoonoses and wildlife: One health, spillover and human activity. Int. J. Parasitol. 2013;43:1079–1088. PubMed PMC

Van Hemert C., Pearce J.M., Handel C.M. Wildlife health in a rapidly changing North: focus on avian disease. Front. Ecol. Environ. 2014;12:548–556. PubMed PMC

Visconti S., Giovannetti L., Canestri-Trotti G. Su di un trematode del genere Cyclocoelum Brandes, 1892, parassita dei sacchi aerei di Turdus merula L. Parassitologia. 1988;30(Suppl. 1):211–212. PubMed

Morishitium polonicum (Machalska, 1980) is a junior synonym of Morishitium dollfusi (Timon-David, 1950) (Trematoda: Cyclocoeliidae)