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.