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).