4 | Discussion
Although many studies have pointed out the negative impacts of parasites on wild host populations, most reported simple correlations and hence overlooked causal relationships (Harper et al ., 1999; Vicenteet al., 2004; Sala-Bozano et al., 2012; Hasegawa et al., 2022a). This is probably due to methodological difficulties in the long-term tracking of host individual and parasite infections. Only two studies have explicitly tested the causality using unique methods, such as haematological inspection and otolith/scale back-calculation (Beldomenico et al., 2008, 2009 a, b; Blanchet et al.,2009). Our study, by contrast, directly monitored the changes in infection intensity, host body condition, growth rate, and survival by the mark-recapture method, and therefore, serves more rigorous evidence of causal relationships and positive feedback in wild populations.
Strikingly, our study showed that both causalities were possible in wild populations, suggesting that positive feedback could occur in wild conditions; parasite infections reduced host conditions, and reduced conditions caused further parasite infections, and so on. The body condition index generally represents the host’s overall health status, energy budget, and immune functions (Wilder et al., 2016; Sánchezet al., 2018). Although hosts commonly cope with parasite infections using innate and adaptive immune systems (Graham et al., 2011; Fast, 2014), developing and maintaining these systems are very costly (Lochmiller, 1996; Sheldon & Verhulst, 1996), and therefore hosts with poor conditions, mainly due to parasite infections, cannot allocate their resources to immunity, resulting in higher parasite intensity. Our study clearly shows this trend.
Behavioural differences dependent on host body condition also explain positive feedback. Animals often show anti-parasite tactics such as dispersal from infection sources (Brown et al., 2016; Teruiet al., 2017) and “parasite-removing behaviours” such as substrate rubbing (Kabata & Cousens, 1977; Atkinson et al.,2018). However, these behaviours are commonly considered energy dependent (Krohn & Boisclair, 1994; Bonte et al., 2012; Teruiet al., 2017); thus, hosts with poor conditions cannot employ these tactics.
How did the copepods in our study cause positive feedback?Salmincola spp. cause tissue damage, such as gill destructions and mouth cavity swellings (Kabata & Cousens, 1977; Nagasawa et al., 1998; Hasegawa et al., 2022a). These infections also induce the immune response of hosts (Hiramatsu et al ., 2001). Beyond developing immune systems, repairing damaged tissues also requires much energy (White et al., 2020), eventually leading to loss of host body condition (Hasegawa et al., 2022a). Physical attachment itself could induce body condition loss. In particular, since our focused copepods mainly attach to the mouth cavity, their infections reduce host foraging activity and strongly reduce host body conditions (Nagasawa et al., 1994). Further, intraspecific competition may play an important role in susceptibility to infections. Poor condition fish are commonly outcompeted by other conspecifics in intra-specific competitions, especially among salmonids with a strong dominance hierarchy (Nakano, 1995). Whereas fish with a high hierarchy dominate at the centre of the flow (Nakano, 1995), outcompeted fish may be forced to move outside of the flow, where free-swimming copepodids may easily attach to the hosts under such low-flow environments (Monzyk et al., 2015). Under these mechanisms, positive feedback can easily occur, as demonstrated in our system.
We found that heavily infected hosts with poor conditions had lower apparent survival rates, suggesting that positive feedback could play important roles in host survival and ultimately undermine the host population (Beldomenico & Begon, 2010). Many studies have shown that heavily infected hosts, generally in poor conditions, tend to have lower survival rates in the wild (Ferguson et al., 2011; Mayo-Hernándezet al ., 2015). Given that body condition is continuously reduced as positive feedback occurs, host body condition eventually fails to meet the threshold for maintaining critical physiological and physical functions such as metabolism. Further, heavily infected hosts with poor conditions are likely to be preyed by predators (Temple, 1987) and outcompeted by conspecifics (Barber et al., 2000; Filipssonet al., 2018). These biological interactions indirectly reduce the host survival rate.
Finally, positive feedback should be carefully taken into account when considering host–parasite dynamics because this concept may also work at the population level (Beldomenico & Begon, 2010). Beldomenico and Begon (2010) predicted that populations with a large proportion of individuals in poor conditions are likely to have a higher prevalence and infection intensity, and this also increases the risk of further infections. Since average body condition and immune ability vary among populations (Cornet et al., 2009; Becker et al., 2020), such predictions are likely to occur in natural systems. Further, positive feedback may eventually cause host death, as discussed above, so this may affect host population dynamics. In this context, the southern salmonid populations, as in the present case, will be threatened by positive feedback. Such populations will especially be vulnerable to increasing water temperature induced by climate change (Nakano et al., 1996) because temperature increment would be stressful for cold water-adopted salmonids and would ultimately decrease their body condition (Peterson et al., 1979; Larsson, 2005). Under such a scenario, the proportion of fish individuals with poor conditions will increase, and parasites will expand more rapidly there. More case studies and monitoring are needed to verify this prediction.