First report of Spirometra (Eucestoda; Diphyllobothriidae) naturally occurring in a fish host

Abstract

Spirometra Faust, Campbell et Kellogg, 1929 is a genus of cestodes belonging to the family Diphyllobothriidae. To date, amphibians, reptiles, and mammals are known second intermediate hosts of these parasites; humans can also be infected (the zoonotic disease is known as sparganosis or spirometrosis). Although the number of phylogenetic studies on Spirometra spp. has increased worldwide in recent years, there are few in South America. Specifically in Uruguay, molecular studies have shown that tapeworms of S. decipiens (Diesing, 1850) complexes 1 and 2 are present in this country. In this study, we characterised the larvae of Spirometra present in the annual fish Austrolebias charrua Costa et Cheffe. Phylogenetic analysis of the cytochrome c oxidase subunit I (COI) sequences of these larvae showed that they belong to S. decipiens complex 1. This is the first report of teleost fishes serving as a second intermediate host for tapeworms of the genus Spirometra in nature.

Diversity and biology of Spirometra tapeworms (Cestoda: Diphyllobothriidea), zoonotic parasites of wildlife: A review

“…This complex 1 consists of specimens of various South American carnivores (adults) and plerocercoids of reptiles and humans, including the enigmatic Sparganum proliferum ( Arrabal et al, 2020 ). Vettorazzi et al (2023) have also indicated the rivulid killifish Austrolebias charrua as paratenic host of this tapeworm, which is the first report of Spirometra plerocercoids in fish.…”

“…Small aquarium fish, catfish ( Ameiurus melas [Rafinesque], Cnidoglanis macrocephalus [Valenciennes], Silurus glanis L.), mosquitofish ( Gambusia affinis Baird et Girard), goldfish ( Carassius auratus [L.]) and rainbow trout ( Oncorhynchus mykiss [Walbaum]) were used unsuccessfully in laboratory experiments ( Joyeux et al, 1934 ; Mueller, 1960 ; Odening and Bockhardt, 1982 ; Stephanson, 1985 ). However, Vettorazzi et al (2023) reported a natural infection of the killifish Austrolebias charrua Costa et Cheffe (Cyprinodontiformes: Rivulidae) in Uruguay. The prevalence of infection was high (up to 58%), but the actual role of killifish in the life cycle of Spirometra tapeworms is not known.…”

“…Representative DNA sequences : Miyadera et al (2001) , Petrigh et al (2015) , Almeida et al (2016) , Arrabal et al (2020) , Armúa-Fernández et al (2021) , Kuchta et al (2021) , Fredes et al (2022) , Kikuchi et al (2021) , Vettorazzi et al (2023) ; Trindade et al unpublished – see the Genbank database).…”

“…Spirometra tapeworms with different names have been found in Argentina, Bolivia, Brazil, Chile, Colombia, Ecuador, Panama, Paraguay, Peru, Suriname, Trinidad, Uruguay and Venezuela ( Supplementary Table S1 ). However, only specimens from Argentina, Bolivia, Brazil, Colombia, Uruguay and Venezuela were sequenced ( Vettorazzi et al, 2023 ).…”

“… Scholz and Kuchta (2016) reviewed zoonotic broad tapeworms (members of Diphyllobothrium and relatives) that use fish as intermediate hosts, while Kuchta et al (2021) presented the first molecular phylogenetic hypothesis on the relationship of the species of Spirometra , whose members can cause life-threatening sparganosis. Species of Spirometra use terrestrial, mainly carnivorous mammals as definitive hosts and amphibians (frogs), reptiles (snakes) and mammals, rarely birds, but almost never fish (see Vettorazzi et al, 2023 and below), as their second intermediate hosts. Sparganosis is a disease of humans and animals caused by (i) ingestion of the first intermediate host (through drinking water with freshwater copepods infected with procercoids), (ii) ingestion of the second intermediate host (mainly snakes or frogs) infected with plerocercoids, or (iii) contact of an open wound with intermediate hosts ( Waeschenbach et al, 2017 ; Kuchta et al, 2021 ).…”