Identification of the avian tracheal trematode Typhlocoelum cucumerinum (Trematoda: Cyclocoelidae) in a host-parasite-environment system: diagnosis, life cycle and molecular phylogeny

Abstract

Typhlocoelum cucumerinum is a tracheal parasite of birds widely distributed across the globe. Nevertheless, aspects of the biology of this cyclocoelid are still poorly understood. Herein, we report the finding of T. cucumerinum in definitive and intermediate hosts from an urban waterbody of Brazil. The parasite was initially detected during the necropsy of domestic Muscovy ducks (Cairina moschata) found dead in the locality. Coproparasitological tests in live animals revealed that 12/47 (25.53%) Muscovy ducks and 2/8 (25%) mallards (Anas platyrhynchos platyrhynchos) were infected with T. cucumerinum. Moreover, rediae and metacercariae morphologically similar to T. cucumerinum were found in 3/248 (1.33%) Biomphalaria straminea collected in the same waterbody frequented by the birds. The conspecificity between the adult and the larval stages was confirmed molecularly (100% similarity in Cox-1). Moreover, the phylogenetic position of T. cucumerinum was determined for the first time based on partial fragments of the 28S, Cox-1 and Nad-1 genes. The species grouped with other members of the subfamily Typhlocoelinae with sequences available, but the data obtained do not support the distinctiveness of the genera Typhlocoelum and Tracheophilus. Further studies involving a broader range of species can result in taxonomic rearrangements in Typhlocoelinae.

Keywords: Typhlocoelinae; domestic waterfowl; life cycle; phylogeny.

Graphical abstract

Fig. 1.

Typhlocoelum cucumerinum found in naturally infected Cairina moschata from Brazil. (A) Alive trematodes found in the trachea during necropsy. (B) Whole view of carmine stained worm. (C) Cirrus sac (arrow). (D) Egg of the parasite containing a developed miracidium. Scale bars: A = 15 mm, B–C = 200 μm, D = 50 μm.

Fig. 2.

Larval stages of Typhlocoelum cucumerinum found in Biomphalaria straminea from an urban lake from Brazil. (A) Redia. (B) Details of anterior end redia. (C) Metacercaria. (D) Cercaria. Scale bars: A = 200 μm, B–D = 50 μm.

Fig. 3.

Phylogenetic relationships between Typhlocoelum cucumerinum and selected members of the family Cyclocoelidae inferred from partial 28S (1170 bp) (A), Cox-1 (343 bp) (B) and Nad-1 (395 bp) (C) sequences analysed by BI and ML methods. Nodal supports are indicated as ML/BI; values smaller than 0.90 for BI and 70 for ML are indicated by a dash. Asterisks indicate nodes that were not found in ML. New sequences from the current study are shown in bold.