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Human activities have increased the intensity and frequency of natural stressors and created novel stressors, altering host–pathogen interactions and changing the risk of emerging infectious diseases. Despite the ubiquity of such anthropogenic impacts, predicting the directionality of outcomes has proven challenging. Here, we conduct a review and meta‐analysis to determine the primary mechanisms through which stressors affect host–pathogen interactions and to evaluate the impacts stress has on host fitness (survival and fecundity) and pathogen infectivity (prevalence and intensity). We assessed 891 effect sizes from 71 host species (representing seven taxonomic groups) and 78 parasite taxa from 98 studies. We found that infected and uninfected hosts had similar sensitivity to stressors and that responses varied according to stressor type. Specifically, limited resources compromised host fecundity and decreased pathogen intensity, while abiotic environmental stressors (e.g., temperature and salinity) decreased host survivorship and increased pathogen intensity, and pollution increased mortality but decreased pathogen prevalence. We then used our meta‐analysis results to develop susceptible–infected theoretical models to illustrate scenarios where infection rates are expected to increase or decrease in response to resource limitations or environmental stress gradients. Our results carry implications for conservation and disease emergence and reveal areas for future work.
Predicting and disrupting transmission of human parasites from wildlife hosts or vectors remains challenging because ecological interactions can influence their epidemiological traits. Human schistosomes, parasitic flatworms that cycle between freshwater snails and humans, typify this challenge. Human exposure risk, given water contact, is driven by the production of free-living cercariae by snail populations. Conventional epidemiological models and management focus on the density of infected snails under the assumption that all snails are equally infectious. However, individual-level experiments contradict this assumption, showing increased production of schistosome cercariae with greater access to food resources. We built bioenergetics theory to predict how resource competition among snails drives the temporal dynamics of transmission potential to humans and tested these predictions with experimental epidemics and demonstrated consistency with field observations. This resource-explicit approach predicted an intense pulse of transmission potential when snail populations grow from low densities, i.e., when per capita access to resources is greatest, due to the resource-dependence of cercarial production. The experiment confirmed this prediction, identifying a strong effect of infected host size and the biomass of competitors on per capita cercarial production. A field survey of 109 waterbodies also found that per capita cercarial production decreased as competitor biomass increased. Further quantification of snail densities, sizes, cercarial production, and resources in diverse transmission sites is needed to assess the epidemiological importance of resource competition and support snail-based disruption of schistosome transmission. More broadly, this work illustrates how resource competition can sever the correspondence between infectious host density and transmission potential.more » « less
Hosts and their parasites exist within complex ecological communities. However, the role that non‐focal community members, species which cannot be infected by a focal pathogen, may play in altering parasite transmission is often only studied in the lens of the ‘diversity‐disease’ relationship by focusing on species richness. This approach largely ignores mechanistic species interactions and risks collapsing our understanding of the community ecology of disease down to defining the prominence of ‘amplification’ versus ‘dilution’ effects.
However, non‐focal species vary in their traits, densities and types of interactions with focal hosts and parasites. Therefore, a community ecology approach based on the mechanisms underlying parasite transmission, host harm and dynamic species interactions may better advance our understanding of parasite transmission in complex communities.
Using the concept of the parasite's basic reproductive ratio,
R0, as a generalizable framework, we examine several critical mechanisms by which interactions among hosts, parasites and non‐focal species modulate transmission and provide examples from relevant literature.
By focusing on the mechanism by which non‐focal species impact transmission, we can emphasize the similarities among classic paradigms in the community ecology of disease, gain new insights into parasite invasion and persistence, better predict community traits correlated with disease dilution or amplification, and gauge the feasibility of biocontrol for parasites of conservation, agricultural or human health concern.
Plain Language Summarycan be found within the Supporting Information of this article.
Abstract Batrachochytrium dendrobatidis(Bd) has been associated with massive amphibian population declines worldwide. Wildlife vaccination campaigns have proven effective for mitigating damage from other pathogens, and there is evidence that adult frogs can acquire resistance to Bd when exposed to killed Bd zoospores and the metabolites they produced.
Here, we investigated whether Cuban treefrogs tadpoles
Osteopilus septentrionaliscan gain protection from Bd through exposure to a prophylaxis treatment composed of killed zoospores or soluble Bd metabolites. We used a 2 × 2 factorial design, crossing the presence or absence of killed zoospores with the presence or absence of Bd metabolites. All hosts were subsequently exposed to live Bd to evaluate susceptibility.
Exposure to killed zoospores did not induce a protective response. However, tadpoles exposed to Bd metabolites had significantly lower Bd intensity and prevalence than tadpoles that were not exposed to metabolites.
The metabolites Bd produce pose no risk of Bd infection and therefore make an epidemiologically safe prophylaxis treatment, protecting tadpoles against Bd. This work provides a promising potential for protecting amphibians in the wild as a disease management strategy for controlling Bd‐associated declines.
Temperature constrains the transmission of many pathogens. Interventions that target temperature-sensitive life stages, such as vector control measures that kill intermediate hosts, could shift the thermal optimum of transmission, thereby altering seasonal disease dynamics and rendering interventions less effective at certain times of the year and with global climate change. To test these hypotheses, we integrated an epidemiological model of schistosomiasis with empirically determined temperature-dependent traits of the human parasite
Schistosoma mansoniand its intermediate snail host ( Biomphalariaspp.). We show that transmission risk peaks at 21.7 °C ( T opt), and simulated interventions targeting snails and free-living parasite larvae increased T optby up to 1.3 °C because intervention-related mortality overrode thermal constraints on transmission. This T optshift suggests that snail control is more effective at lower temperatures, and global climate change will increase schistosomiasis risk in regions that move closer to T opt. Considering regional transmission phenologies and timing of interventions when local conditions approach T optwill maximize human health outcomes.
Agricultural expansion is predicted to increase agrochemical use two to fivefold by 2050 to meet food demand. Experimental evidence suggests that agrochemical pollution could increase snails that transmit schistosomiasis, a disease impacting 250 million people, yet most agrochemicals remain unexamined.
Here we experimentally created >100 natural wetland communities to quantify the relative effects of fertilizer, six insecticides (chlorpyrifos, terbufos, malathion, λ‐cyhalothrin, permethrin and esfenvalerate), and six herbicides (acetochlor, alachlor, metolachlor, atrazine, propazine and simazine) on two snail genera responsible for 90% of global schistosomiasis cases.
We identified four of six insecticides (terbufos, permethrin, chlorpyrifos and esfenvalerate) as high risk for increasing snail biomass by reducing snail predators. Hence, malathion and λ‐cyhalothrin might be useful for improving food production without increasing schistosomiasis. This top‐down effect of insecticides on predators was so strong that the effects of herbicides on schistosomiasis risk were masked in the presence of predators because there were so few snails. In the absence of snail predators, herbicide effects on snails were generally negative by reducing submerged vegetation
Hydrilla verticillata. The exception was that atrazine and acetochlor significantly increased the biomass of infected snails and total snails respectively.
Like insecticides, fertilizer had strong positive effects on snail populations. Fertilizer increased both snail habitat (submerged vegetation) and snail food (periphyton), but of these two pathways, the increases in snail habitat resulted in greater snail population growth. Total snail biomass was positively associated with both infected snail biomass and parasite production and thus human infection risk.
Synthesis and applications. Our findings suggest that fertilizers and insecticides generally have consistently higher chances of increasing human schistosomiasis than herbicides in natural communities. Furthermore, our results highlight the need to identify other low risk insecticides, which might help reduce crop pests without increasing snails and thus risk of schistosomiasis.