Stressors modulate host density
A key assumption of many infectious disease models is that contact rates
between infected and uninfected individuals increase as population
density increases (Anderson et al. 1986; McCallum et al.2001). Therefore, if stressors negatively impact host fitness by
restricting host population growth via reduced fecundity or increased
mortality or emigration, pathogens will be less frequently transmitted,
and prevalence is expected to decline. This reasoning justifies culling
campaigns, where infection rates are reduced or pathogens are extirpated
by reducing host density below a critical transmission threshold
(Lafferty & Holt 2003; Prentice et al. 2019). Although, to our
knowledge, no studies have explicitly evaluated the
stressor-density-disease relationship, studies have shown that human
pressures indirectly increase host-density thresholds resulting in
epidemics. For instance, overfishing of predatory lobsters
(Panulirus interruptus ) has led to dense purple urchin
(Strongylocentrotus purpuratus ) populations, more likely to
experience urchin-specific bacterial (Vibrio bacteria) epidemics
(Lafferty 2004). Similarly, although thermal stress increases the
susceptibility of corals to disease, it only leads to white syndrome
outbreaks where corals are at high density (Bruno et al. 2007).
Alternatively, stressors may contribute to increased local host density
without increasing fecundity. For instance, behavioral responses to
stressors, such as changes in migration patterns (Satterfield et
al. 2018; Sánchez et al. 2020), foraging behaviors (Epsteinet al. 2006), and aggregations in low-quality food-provisioned
sites (intentional or unintentional) (Becker et al. 2015), have
been associated with higher host density. Consequently, higher local
density may intensify disease transmission via increased contact rates,
as illustrated by theoretical models (Becker & Hall 2014).
Disease transmission can also be sustained at low population density.
For instance, in social species, the frequency of social contact can
govern disease epidemics independently of host density (Johnson et
al. 2011; Rimbach et al. 2015; Rushmore et al. 2017).
Given that density-independent transmission (e.g., sexual or
vector-borne transmission) does not require a minimum host density for
parasites to invade a population (Hopkins et al. 2020), it is
expected that a combination of stressors and pathogen infection would
drive populations to extinction more frequently than density-dependent
transmissions (Castro et al. 2005; Ryder et al. 2007).
Stressors may affect the fitness of infected and uninfected hosts
differently. Infection increases sensitivity to other stressors, as
infected hosts are more energetically constrained (Marcogliese &
Pietrock 2011). Such a combined effect of stress (warming temperatures)
and infection (e.g., Vibrio coralliilyticus ) may be responsible
for the rapid global coral reef decline (Maynard et al. 2015).
Despite many examples of synergistic tolls that stressors and pathogens
have on host fitness (Crain et al. 2008), few have tested whether
stressors have a differential impact on the fitness of infected compared
to uninfected hosts (Marcogliese & Pietrock 2011; Beldomenico & Begon
2016).