1 | Introduction
Parasites account for more than one-third of species on Earth and a
great deal of biomass in ecosystems (Lafferty et al., 2006;
Dobson et al ., 2008; Kuris et al., 2008); hence,
host–parasite relationships are one of the most common biotic
associations in nature (Hudson et al., 2006; Dobson et
al ., 2008; Kuris et al ., 2008). Parasites damage host health via
directly exploiting resources from hosts or indirectly causing
physiological burdens (Poulin, 2011; Sheldon & Verhulst, 1996) and can
be major drivers of host evolutionary changes (Paterson et al.,2010) and host population dynamics (Hudson et al ., 1998; Poulin,
2011). Parasite infections also occur as a consequence of poor host
health (Lochmiller, 1996; Pederson & Greives, 2008; Beldomenicoet al ., 2008). Given that gaining or maintaining immunity is
nutritionally costly for hosts (Lochmiller, 1996; Sheldon & Verhulst,
1996), host individuals without enough available food resources can be
easily predisposed to higher parasite loads (Forbes et al .,
2016). These opportunistic infections in epidemiology may cause parasite
outbreaks and finally crush wild populations (Lochmiller, 1996).
Therefore, parasite infections and host health synergistically affect
wild host and parasite dynamics.
Elucidating the synergy of parasite infections and host body conditions
in the wild can advance our understanding of wild host population
dynamics. However, most field studies have only examined cross-sectional
correlations and have discussed one-sided causalities (Beldomenicoet al ., 2008). Field studies suggest a negative correlation
between host body condition, and infection parameters generally indicate
that parasites are causes of poor host condition (Harper et al .,
1999; Vicente et al., 2004; Sala-Bozano et al., 2012;
Hasegawa et al., 2022a), although some showed poor condition
situations such as food limitations may increase parasite prevalence and
intensity because hosts compromise their immune functions under such
situations (Forbes et al., 2016). Most importantly, when parasite
infections are both the cause and consequence of a poor host condition,
we can also expect positive feedback: an infected host with a poor body
condition due to the parasite infection will be more susceptible to
further infection (Beldomenico et al., 2008; Beldomenico et
al., 2009 a, b; Beldomenico & Begon, 2010). Positive feedback may
create heavily infected hosts, which could be “super spreaders” among
the populations (Beldomenico & Begon, 2010). Further, positive feedback
can decrease host survival and eventually undermine the host population
(Beldomenico & Begon, 2010).
Both causalities and positive feedback are likely to occur but have
rarely been demonstrated in natural populations. This is probably
because tracking small and cryptic parasite infections is usually
difficult without sacrificing host individuals, although longitudinal
studies are one of the best ways to estimate the causalities in natural
systems (Beldomenico et al., 2008; Telfer et al., 2010).
Only a few studies have overcome these problems and specifically tested
their causalities in wild conditions. A series of studies by Beldomenicoet al. (2008, 2009a, 2009b) successfully detected parasite
infections on field voles Microtus agrestis in the field using a
haematological method, and they monitored the infection status and host
body condition combined with mark-recapture analysis of the host,
clearly demonstrating positive feedback. A haemogram can be a useful
indicator of infection; however, the authors did not observe parasites
directly in the blood, and specific changes in infection intensity were
not clarified. Blanchet et al. (2009) also demonstrated the
causal relationships between parasite infections and host growth rates
by estimating the growth of two host fishes from scales and otoliths,
although these methods have potential estimation errors (e.g. Neilson,
1992), and the duration, frequency, and intensity of parasites before
sampling were unknown. Moreover, these previous studies failed to
evaluate host survival rate, even though positive feedback could likely
cause host death in natural populations and, hence, affect wild host
population dynamics (Beldomenico & Begon, 2010). Thus, previous
findings have not sufficiently demonstrated the existence of
condition–infection causality and positive feedback, necessitating more
rigorous empirical evidence.
Here, we provide the first rigorous evidence of both causalities and
positive feedback in wild populations by using a mark-recapture survey
combined with structural equation modelling (SEM) in a wild stream
fish–parasitic copepod system. SEM analysis is a powerful method for
estimating the causalities in longitudinal datasets because of its
simplicity and robustness (Fan et al., 2016). In fact, several
studies have applied this approach to longitudinal studies and have
revealed complex natural interactions (Almaraz, 2005; Byrnes et
al., 2011). Our focused ectoparasitic copepod, Salmincolacf. markewitschi , is ideal for examining the causality between
host body condition and parasite numbers because of their relatively
large body size (2–5 mm; Kabata, 1969) and characteristic of attaching
to the mouth cavities of host salmonid, white-spotted charr (Kabata,
1969), enabling us to track the change in infection intensity and host
body condition longitudinally without sacrificing host fish. Further,
previous studies have suggested that Salmincola spp. have
negative impacts on host fitness components under rearing conditions,
such as decline of fecundity (Gall et al., 1972), appetite
(Nagasawa et al., 1994; Hiramatsu et al., 2001), and body
condition (Nagasawa et al., 1998). Our previous studies also
showed clear negative correlations between Salmincola cf.markewitschi loads and fish conditions in natural streams (Figure
1; Hasegawa & Koizumi under review 1). We conducted a mark-recapture
survey of white-spotted charr Salvelinus leucomaenis andSalmincola cf. markewitschi infecting the host mouth
cavity in the Shiodomari River in southern Hokkaido. We also evaluated
the apparent survival rate of host fish during the mark-recapture period
to assess whether positive feedback reduces host survival in the wild.