Elucidation of the life cycle of Galactosomum nagasakiense (Heterophyidae), the causative parasite of trematode whirling disease in marine fish, with discovery of congeneric species in the gastropod first intermediate host Cerithium dialeucum.

Abstract

Trematode whirling disease (TWD), caused by Galactosomum nagasakiense (Heterophyidae), affects a wide range of wild and cultured marine fish, with occasional mass mortalities reported in aquaculture since the 1960s. Fish serve as the second intermediate host, while the black-tailed gull Larus crassirostris has been identified as the definitive host. However, the first intermediate host has remained unidentified for decades. Field surveys were conducted in Tsushima, Nagasaki Prefecture, Japan, an endemic region of TWD, aiming to identify the gastropod first intermediate host. Among 1341 snails sampled, trematode infections were detected in 15 individuals of the cerithiid snail, Cerithium dialeucum (n = 798, prevalence = 1.9 %). Three morphologically distinct types of magnacercous cercariae were isolated from C. dialeucum, and molecular analysis confirmed that all types belonged to the genus Galactosomum. The nuclear ITS2 and 28S rDNA sequences of the most prevalent type (detected in 11 out of the 15 infected C. dialeucum) were 100 % identical to sequences obtained from metacercariae found in the brain of TWD-affected fish, confirming its identity as G. nagasakiense. The remaining two types were assigned to the genus Galactosomum based on both morphological and genetical characteristics but could not be identified to the species level. Morphological descriptions of the cercaria and redia of G. nagasakiense are provided. The cercariae exhibited strong positive phototaxis and swam actively using a long, unforked tail. A single infected snail released up to 3000 cercariae per day. This study identifies, for the first time, the first intermediate host of G. nagasakiense, thereby completing the elucidation of its life cycle.