The oceanic pleuston community as a potentially crucial life-cycle pathway for pelagic fish-infecting parasitic worms

Pleustonic organisms form an important part of pelagic ecosystems by contributing to pelagic trophic chains and supporting connectivity between oceanic habitats. This study systematically analysed the trematode community harboured by pleustonic molluscs and cnidarians from offshore Queensland, Australia. Four mollusc and three cnidarian species were collected from beaches of North Stradbroke Island, Queensland. Two mollusc species and all three cnidarians harboured large numbers of hemiuroid metacercariae (Trematoda: Hemiuroidea). Eight taxa from four hemiuroid families (Accacoeliidae, Didymozoidae, Hemiuridae and Sclerodistomidae) were distinguished via molecular sequencing. Four of those taxa were identified to species. All trematode taxa except one didymozoid were shared by two or more host species; five species occurred in both gastropods and cnidarians. It is hypothesised that the life-cycles of these hemiuroids are highly plastic, involving multiple opportunistic pathways of metacercarial transmission to the definitive hosts. Transmission and the use of pleuston by hemiuroids likely varies with sea surface use and ontogenetic trophic shifts of apex predators. The small number of trematode species found in pleuston is consistent with significant ecological specificity, and the inference that other pelagic trematodes use alternative pathways of transmission that do not involve pleustonic organisms. Such pathways may involve i) pelagic hosts exclusively; ii) benthic or demersal hosts exclusively, consumed by apex predators during their dives; or iii) both benthic and pelagic hosts in transmission chains dependent on vertical migrations of prey. The influence of the connectivity of open-ocean ecosystems on parasite transmission is identified as an area in critical need of research.