Future directions and concluding remarks
Our analysis included all experimental studies, with hosts exposed to a
single parasite species and a single stressor. This approach, although
easier to interpret and valuable to tease apart the effects of a
stressor in host-pathogen interactions, is difficult to translate to the
natural world, where populations are likely exposed to multiple
parasites and a combination of stressors. When considering
co-infections, for instance, stressors might compromise one arm of
immune defense, making hosts more vulnerable to pathogens that require
such response. For example, food restriction increased levels of
eosinophils in capybaras (a Th2 immune response) and consequently
reduced nematode burden (which resistance relies on the Th2 response),
but coccidian infection intensity increased due to inadequate Th1 immune
response (Eberhardt et al. 2013). Future studies should use a
combination of field and laboratory experiments to perturb processes
that covary with stressors to determine how and why results vary
comparing laboratory and real-world conditions.
As a next level of complexity, host-pathogen systems do not occur in
isolation, and some other biotic stressors and interactions can
indirectly affect disease dynamics. For example, hosts compete for
resources with other species and are consumed by predators.
Consequently, stressors can affect other community members in ways that
could enhance or negate epidemiological effects on hosts and pathogens
(Strauss et al. 2015, 2016). Furthermore, most known parasites
infect multiple host species (Woolhouse et al. 2001), but some
host species are disproportionately responsible for parasite
transmission (Haydon et al. 2002). Generally, ecologically
resilient species exhibit fast life histories and invest relatively less
in immune defense compared to more disturbance-sensitive species
(Johnson et al. 2012; Previtali et al. 2012; Pap et
al. 2015), predicting that resilient species will have an insufficient
immune response to prevent pathogen replication and transmission,
resulting in higher transmission rates. Therefore, future research is
sorely needed to evaluate the effects stressors have on different host
species and their relative contribution to community disease
transmission.
Moreover, combining experimental and modeling approaches is needed to
move beyond associational patterns and to a mechanistic understanding of
how stressors affect hosts and pathogens due to the common occurrence of
multiple simultaneous stressors. Approaches are available for
incorporating stressors into epidemiological models, such as examining
variation in R0, the basic reproductive number of a
parasite (Anderson & May 1991). Pinpointing when and how stressors
increase or decrease R0 represents a crucial first step
toward understanding their roles in the dynamics of infectious diseases.
Yet even though multiple mechanisms (including changes in host contact
rates and per-contact probability of transmission) are often subsumed in
the transmission parameter β, these need not be fixed, as we have
illustrated with our models. The same applies to birth and death rates,
and even to parasite virulence, given that variation in host immune
defenses alters per-contact transmission probabilities and the duration
of the infectious period. As a next step, integrating a series of models
with empirical results will inform the generality of the predicted
patterns.
Finally, our study also highlights the need to expand empirical research
at the interface of stress and infectious disease in highly relevant
systems for zoonotic disease emergence. The studies included in our
meta-analysis had low coverage of both vertebrates and terrestrial
systems, yet terrestrial vertebrates such as rodents and bats have been
linked repeatedly to zoonotic diseases affecting humans and livestock
(Luis et al. 2013; Han et al. 2016). However, only one
study of rodents provided sufficient data to be included in our
meta-analysis (Eze et al. 2013).
As anthropogenic activities continue to alter ecosystems in ways that
facilitate disease emergence worldwide, we must consider the effects
stressors have on disease dynamics. Our findings improve our
understanding of this interplay and provide insights for predicting and
mitigating the impacts of stressor-pathogen synergies on human, animal,
and planetary health.