Species interactions may profoundly influence disease outbreaks. However, disease ecology has only begun to integrate interactions between hosts and their food resources (foraging ecology) despite that hosts often encounter their parasites while feeding. A zooplankton-fungal system illustrated this central connection between foraging and transmission. Using experiments that varied food density for Daphnia hosts, density of fungal spores and body size of Daphnia, we produced mechanistic yet general models for disease transmission rate based on broadly applicable components of feeding biology. Best performing models could explain why prevalence of infection declined at high food density and rose sharply as host size increased (a pattern echoed in nature). In comparison, the classic mass-action model for transmission performed quite poorly. These foraging-based models should broadly apply to systems in which hosts encounter parasites while eating, and they will catalyse future integration of the roles of Daphnia as grazer and host.

Seasonal change in the intensity of fish predation affects succession in lake zooplankton communities. Predation affects not only the zooplankton prey, but also their parasites. Because the ability of a parasite to spread depends in part on the death rate of the hosts, seasonal reductions in the intensity of predation on zooplankton could lead to parasite epidemics. We examined seasonal population dynamics, mortality rate, and incidence of parasitism in lake populations of Daphnia to determine whether parasitism displayed seasonality and synchrony among lake populations and whether any such patterns are consistent with seasonal changes in predation rates. Infections of a bacterial parasite (Spirobacillus cienkowskii) in Daphnia dentifera populations were seasonal with epidemics in many lakes occurring synchronously in autumn. In situ foraging behavior of the dominant fish planktivores, bluegill sunfish, is highly selective on infected Daphnia. Mortality rates on the Daphnia drop just prior to the initiation of epidemics. An epidemiological model shows that this magnitude of decrease in mortality rate, if driven largely by a reduction in predation, can account for the seasonal occurrence of epidemics in our Daphnia populations. Together, these results suggest that parasitism in Daphnia populations may be seasonally restricted by fish predation.Historically, ecologists studying food webs regarded parasites as add-ons (Marcogliese and Cone 1997), while ecologists studying parasitism focused on the isolated interactions of hosts and parasites. Yet the ability of a parasite to spread and persist in a host population depends critically on the other members of the community (e.g., competitors and predators;Packer et al. 2003).

Climatic warming will likely have idiosyncratic impacts on infectious diseases, causing some to increase while others decrease or shift geographically. A mechanistic framework could better predict these different temperature-disease outcomes. However, such a framework remains challenging to develop, due to the nonlinear and (sometimes) opposing thermal responses of different host and parasite traits and due to the difficulty of validating model predictions with observations and experiments. We address these challenges in a zooplankton-fungus (Daphnia dentifera-Metschnikowia bicuspidata) system. We test the hypothesis that warmer temperatures promote disease spread and produce larger epidemics. In lakes, epidemics that start earlier and warmer in autumn grow much larger. In a mesocosm experiment, warmer temperatures produced larger epidemics. A mechanistic model parameterized with trait assays revealed that this pattern arose primarily from the temperature dependence of transmission rate (β), governed by the increasing foraging (and, hence, parasite exposure) rate of hosts (f). In the trait assays, parasite production seemed sufficiently responsive to shape epidemics as well; however, this trait proved too thermally insensitive in the mesocosm experiment and lake survey to matter much. Thus, in warmer environments, increased foraging of hosts raised transmission rate, yielding bigger epidemics through a potentially general, exposure-based mechanism for ectotherms. This mechanistic approach highlights how a trait-based framework will enhance predictive insight into responses of infectious disease to a warmer world.

Coinfection of host populations alters pathogen prevalence, host mortality, and pathogen evolution. Because pathogens compete for limiting resources, whether multiple pathogens can coexist in a host population can depend on their within-host interactions, which, in turn, can depend on the order in which pathogens infect hosts (within-host priority effects). However, the consequences of within-host priority effects for pathogen coexistence have not been tested. Using laboratory studies with a coinfected zooplankton system, we found that pathogens had increased fitness in coinfected hosts when they were the second pathogen to infect a host, compared to when they were the first pathogen to infect a host. With these results, we parameterized a pathogen coexistence model with priority effects, finding that pathogen coexistence (1) decreased when priority effects increased the fitness of the first pathogen to arrive in coinfected hosts and (2) increased when priority effects increased the fitness of the second pathogen to arrive in coinfected hosts. We also identified the natural conditions under which we expect within-host priority effects to foster coexistence in our system. These outcomes were the result of positive or negative frequency dependence created by feedback loops between pathogen prevalence and infection order in coinfected hosts. This suggests that priority effects can systematically alter conditions for pathogen coexistence in host populations, thereby changing pathogen community structure and potentially altering host mortality and pathogen evolution via emergent processes.

Community ecology can link habitat to disease via interactions among habitat, focal hosts, other hosts, their parasites, and predators. However, complicated food web interactions (i.e., trophic interactions among predators and their impacts on host density and diversity) often obscure the important pathways regulating disease. Here, we disentangle community drivers in a case study of planktonic disease, using a two-step approach. In step one, we tested univariate field patterns linking community interactions directly to two disease metrics. Density of focal hosts (Daphnia dentifera) was related to density but not prevalence of fungal (Metschnikowia bicuspidata) infections. Both disease metrics appeared to be driven by selective predators that cull infected hosts (fish, e.g., Lepomis macrochirus), sloppy predators that spread parasites while feeding (midges, Chaoborus punctipennis), and spore predators that reduce contact between focal hosts and parasites (other zooplankton, especially small-bodied Ceriodaphnia sp.). Host diversity also negatively correlated with disease, suggesting a dilution effect. However, several of these univariate patterns were initially misleading, due to confounding ecological links among habitat, predators, host density, and host diversity. In step two, path models uncovered and explained these misleading patterns, and grounded them in habitat structure (refuge size). First, rather than directly reducing infection prevalence, fish predation drove disease indirectly through changes in density of midges and frequency of small spore predators (which became more frequent in lakes with small refuges). Second, small spore predators drove the two disease metrics through fundamentally different pathways: they directly reduced infection prevalence, but indirectly reduced density of infected hosts by lowering density of focal hosts (likely via competition). Third, the univariate diversity-disease pattern (signaling a dilution effect) merely reflected the confounding direct effects of these small spore predators. Diversity per se had no effect on disease, after accounting for the links between small spore predators, diversity, and infection prevalence. In turn, these small spore predators were regulated by both size-selective fish predation and refuge size. Thus, path models not only explain each of these surprising results, but also trace their origins back to habitat structure.

Humans have contributed to the increased frequency and severity of emerging infectious diseases, which pose a significant threat to wild and domestic species, as well as human health. This review examines major pathways by which humans influence parasitism by altering (co)evolutionary interactions between hosts and parasites on ecological timescales. There is still much to learn about these interactions, but a few well-studied cases show that humans influence disease emergence every step of the way. Human actions significantly increase dispersal of host, parasite and vector species, enabling greater frequency of infection in naive host populations and host switches. Very dense host populations resulting from urbanization and agriculture can drive the evolution of more virulent parasites and, in some cases, more resistant host populations. Human activities that reduce host genetic diversity or impose abiotic stress can impair the ability of hosts to adapt to disease threats. Further, evolutionary responses of hosts and parasites can thwart disease management and biocontrol efforts. Finally, in rare cases, humans influence evolution by eradicating an infectious disease. If we hope to fully understand the factors driving disease emergence and potentially control these epidemics we must consider the widespread influence of humans on host and parasite evolutionary trajectories. This article is part of the themed issue ‘Human influences on evolution, and the ecological and societal consequences’.

As natural enemies, parasites can dramatically harm host populations, and even catalyze their decline. Thus, identifying factors that promote disease spread is paramount. Environmental factors can drive epidemics by altering traits involved in disease spread. For example, nutrients (such as nitrogen and phosphorus) can stimulate reproduction of both hosts and parasites or alter rates of disease transmission by stimulating productivity and nutrition of food resources of hosts. Here, we demonstrate nutrient-trait-epidemic connections between the greatly understudied macronutrient potassium (K) and fungal disease (Metschnikowia bicuspidata) in a zooplankton host (Daphnia dentifera). In a three-year survey, epidemics grew larger in lakes with more potassium. In laboratory assays, potassium enrichment of low-K lake water enhanced both host and parasite reproduction. Parameterized with these data, a model predicted that potassium addition catalyzes disease spread. We confirmed this prediction with an experiment in large mesocosms (6000 L) in a low K-lake: potassium enrichment caused larger epidemics in replicated Daphnia populations. Consequently, the model--data combination mechanistically explained the field pattern and revealed a novel ecological role for the nutrient potassium. Furthermore, our findings highlight the need for further development of theory for nutrient limitation of epidemics. Such theory could help to explain heterogeneous eruptions of disease in space, connect these outbreaks to natural or anthropogenic enrichment of ecosystems, predict the ecological consequences of these outbreaks, and reveal novel strategies for disease management.

Seasonal epidemics erupt commonly in nature and are driven by numerous mechanisms. Here, we suggest a new mechanism that could determine the size and timing of seasonal epidemics: rearing environment changes the performance of parasites. This mechanism arises when the environmental conditions in which a parasite is produced impact its performance-independently from the current environment. To illustrate the potential for "rearing effects", we show how temperature influences infection risk (transmission rate) in a Daphnia-fungus disease system through both parasite rearing temperature and infection temperature. During autumnal epidemics, zooplankton hosts contact (eat) fungal parasites (spores) reared in a gradually cooling environment. To delineate the effect of rearing temperature from temperature at exposure and infection, we used lab experiments to parameterize a mechanistic model of transmission rate. We also evaluated the rearing effect using spores collected from epidemics in cooling lakes. We found that fungal spores were more infectious when reared at warmer temperatures (in the lab and in two of three lakes). Additionally, the exposure (foraging) rate of hosts increased with warmer infection temperatures. Thus, both mechanisms cause transmission rate to drop as temperature decreases over the autumnal epidemic season (from summer to winter). Simulations show how these temperature-driven changes in transmission rate can induce waning of epidemics as lakes cool. Furthermore, via thermally dependent transmission, variation in environmental cooling patterns can alter the size and shape of epidemics. Thus, the thermal environment drives seasonal epidemics through effects on hosts (exposure rate) and the infectivity of parasites (a rearing effect). Presently, the generality of parasite rearing effects remains unknown. Our results suggest that they may provide an important but underappreciated mechanism linking temperature to the seasonality of epidemics.