Positive feedback between parasite infection and poor host body condition reduces host survival in the wild

Host–parasite relationships are ubiquitous on Earth. Although parasites reduce host health, parasite infections also occur due to compromised host health. Both causalities could induce positive feedback, in which infected hosts with poor body conditions may suffer further infection. Such positive feedback could increase host mortality and may finally affect host population dynamics. However, both causalities and how positive feedback affect host population dynamics has rarely been demonstrated in the wild, mainly due to methodological difficulties. Here, we used a mark-recapture survey combined with structural equation modelling (SEM) to examine whether both causalities and positive feedback occurred in a host stream salmonid and parasitic copepod system. We also examined the factors affecting the apparent survival of hosts during the mark-recapture period using a Cormack–Jolly–Seber (CJS) model. Our target parasitic copepod Salmincola markewitschi is relatively large, attaching to the mouth cavity of host white-spotted charr Salvelinus leucomaenis, which enabled long-term tracking in natural conditions without sacrificing either host or parasite. SEM using time-series snapshot data detected simultaneous occurrence of both causalities, that is the parasitic copepods reduced host body condition and host with poorer body condition were more likely infected by parasites, suggesting the positive feedback. Furthermore, the negative effects of parasites on host body condition were more frequently detected compared to the opposite causal link (high susceptibility to infections in hosts with poor body condition), and the strengths of both causal links fluctuated across seasons and initial infection statuses. The CJS model revealed that both parasite infection and poor host condition reduced apparent survival. The mouth-attaching copepods might have reduced host body conditions by altering host foraging behaviour and/or inducing physiological costs such as immunity. High susceptibility in fish with poorer body condition was probably caused by low resource allocations to immunity and behavioural defences against parasites. These direct and indirect processes should incur strong stresses to host fish, finally leading to higher mortality. Our findings provided the first empirical evidence on how positive feedback between parasite infection and reduced host condition could influence the wild host population via reduction of host survival. Heavily infected hosts created by positive feedback may also play important roles in parasite spreading, for example, as a super spreader. Together, positive feedback would thus be important ecological processes to better understand host and parasite dynamics in the wild populations. Read the free Plain Language Summary for this article on the Journal blog.