Future directions and concluding remarks
Our analyses included only 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 stressor effects in
host-pathogen interactions, is difficult to translate to the natural
world, where populations are likely exposed to multiple pathogens and a
combination of stressors. When considering co-infections, for instance,
stressors may 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 (where 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 pathogens
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 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 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 toward 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 is crucial to understanding
their roles in infectious disease dynamics. 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 pathogen 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 predicted patterns.
Finally, our study 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
rodent study 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 stressor
effects 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.