Brain-Encysting Trematodes Increase the Frequency but Reduce the Repeatability of Surfacing Behaviour in Mottled Triplefin

Trophically transmitted parasites play a significant role in shaping food webs, especially in aquatic environments, due to their complex life cycles and transmission through predation. Helminths that use this transmission route, such as trematodes and cestodes, can manipulate host behaviour to increase the likelihood of predation by their next host. Recent research suggests that parasites may not only influence single behavioural traits but also multiple traits simultaneously, affecting both the expression and consistency of behaviours that potentially facilitate parasite transmission. To further test this hypothesis, our study examines the impact of the recently discovered brain-encysting trematode Cardiocephaloides ovicorpus on the behaviour and repeatability of personality traits in the mottled triplefin (Forsterygion capito) in Otago Harbour, New Zealand. Naturally infected fish were tested for seven behavioural traits, including exploration, observation, predator avoidance, boldness, surfacing, activity (tank crossing), and aggressiveness, across two trial days. Of the behavioural traits investigated, surfacing was the only one that showed a significant positive correlation with C. ovicorpus infection. Furthermore, our statistical model suggested a decrease in repeatability for this trait as a function of C. ovicorpus infection. It is possible that C. ovicorpus specifically targets the brain region responsible for controlling surfacing, as the increase in surfacing may expose fish to a higher risk of detection by avian predators, the parasite's definitive hosts. Additionally, a decrease in behavioural repeatability may increase the likelihood of mismatches between behavioural responses and stimuli, such as predator cues, further elevating predation risk. Future research could aim to uncover the complete life cycle of C. ovicorpus by identifying the unknown first intermediate host, enabling experimental infections of fish to determine the causal relationship between behavioural variation and parasite infection.