Invisible Parasites and Their Implications for Coexisting Water Fleas.

The top-down effects of consumers, such as predators, are known to affect abundances, size structure, and species composition in aquatic ecosystems. Parasites are also important in shaping the ecology of free-living species; however, their effects are often overlooked because parasites can be difficult to detect. Parasites can be particularly challenging to observe in zooplankton hosts because of their small size and ephemeral infection periods. To overcome these challenges, we used a quarantine approach combined with high-magnification microscopy to increase detection of parasites of the tropical Cladoceran, Ceriodaphnia cornuta, in Lake Gatun, Panamá. Using this approach, we were able to demonstrate that competing morphs of Ceriodaphnia experience differential rates of infection, where the subordinate competitor suffered higher parasite prevalence than did the dominant morph. Predation by fishes on the dominant morph is considered the principal mechanism for their coexistence, but we hypothesize that parasites may also play a role in maintaining morphotype diversity of Ceriodaphnia.

Effects of Intrinsic and Extrinsic Host Mortality on Disease Spread.

The virulent effects of a pathogen on host fecundity and mortality (both intrinsic and extrinsic mortality due to predation) often increase with the age of infection. Age of infection often is also correlated with parasite fitness, in terms of the number of both infective propagules produced and the between-host transmission rate. We introduce a four-population partial differential equations (PDE) model to investigate the invasibility and prevalence of an obligately killing fungal parasite in a zooplankton host as they are embedded in an ecological network of predators and resources. Our results provide key insights into the role of ecological interactions that vary with the age of infection. First, selective predation, which is known both theoretically and empirically to reduce disease prevalence, does not always limit disease spread. This condition dependency relies on the timing and intensity of selective predation and how that interacts with the direct effects of the parasite on host mortality. Second, low host resources and intense predation can prevent disease spread, but once conditions allow the invasion of the parasite, the qualitative dynamics of the system do not depend on the intensity of the selective predation. Third, a comparison of the PDE model with a model based on ordinary differential equations (ODE model) reveals a parametrization for the ODE version that yields an endemic steady state and basic reproductive ratio that are identical to those in the PDE model. Our results highlight the complexity of resource-host-parasite-predator interactions and suggest the need for additional data-theory coupling exploring how community ecology influences the spread of infectious diseases.

Plasticity, not genetic variation, drives infection success of a fungal parasite.

Hosts strongly influence parasite fitness. However, it is challenging to disentangle host effects on genetic vs plasticity-driven traits of parasites, since parasites can evolve quickly. It remains especially difficult to determine the causes and magnitude of parasite plasticity. In successive generations, parasites may respond plastically to better infect their current type of host, or hosts may produce generally 'good' or 'bad' quality parasites. Here, we characterized parasite plasticity by taking advantage of a system in which the parasite (the yeast Metschnikowia bicuspidata, which infects Daphnia) has no detectable heritable variation, preventing rapid evolution. In experimental infection assays, we found an effect of rearing host genotype on parasite infectivity, where host genotypes produced overall high or low quality parasite spores. Additionally, these plastically induced differences were gained or lost in just a single host generation. Together, these results demonstrate phenotypic plasticity in infectivity driven by the within-host rearing environment. Such plasticity is rarely investigated in parasites, but could shape epidemiologically important traits.

Complex Daphnia interactions with parasites and competitors.

Species interactions can strongly influence the size and dynamics of epidemics in populations of focal hosts. The "dilution effect" provides a particularly interesting type of interaction from a biological standpoint. Diluters - other host species which resist infection but remove environmentally-distributed propagules of parasites (spores) - should reduce disease prevalence in focal hosts. However, diluters and focal hosts may compete for shared resources. This combination of positive (dilution) and negative (competition) effects could greatly complicate, even undermine, the benefits of dilution and diluter species from the perspective of the focal host. Motivated by an example from the plankton (i.e., zooplankton hosts, a fungal parasite, and algal resources), we study a model of dilution and competition. Our model reveals a suite of five results: • A diluter that is a superior competitor wipes out the host, regardless of parasitism. Although expected, this outcome is an ever-present danger in strategies that might use diluters to control disease. • If the diluter is an inferior competitor, it can reduce disease prevalence, despite the competition, as parameterized in our model. However, competition may also reduce density of susceptible hosts to levels below that seen in focal host-parasite systems alone. • As they decrease disease prevalence, diluters destabilize dynamics of the focal host and their resources. Thus, diluters undermine the stabilizing effects of disease. • The four species combination can generate very complex dynamics, including period-doubling bifurcations and torus (Neimark-Sacker) bifurcations. • At lower resource carrying capacity, the diluter's dilution of spores is 'helpful' to the focal host, i.e., dilution can elevate host density by reducing disease. But, as the resource carrying capacity increases further, the equilibrium density of the diluter increases while the density of the focal host decreases, despite competition. Namely, the negative effects of competition start to outweigh the positive effects of dilution from the perspective of equilibrium density of the focal host.

Physical structure of lakes constrains epidemics in Daphnia populations.

Parasites are integral parts of most ecosystems, yet attention has only recently focused on how community structure and abiotic factors impact host-parasite interactions. In lakes, both factors are influenced by habitat morphology. To investigate the role of habitat structure in mediating parasitism in the plankton, we quantified timing and prevalence of a common microparasite (Metschnikowia bicuspidata) in its host, Daphnia dentifera, in 18 lakes that vary in basin size and shape. Over three years, we found substantial spatial and temporal variation in the severity of epidemics. Although infection rates reached as high as 50% in some lakes, they did not occur in most lakes in most years. Host density, often considered to be a key determinant of disease spread, did not explain a significant amount of variation in the occurrence of epidemics. Furthermore, host resistance does not fully explain this parasite's distribution, since we easily infected hosts in the laboratory. Rather, basin shape predicted epidemics well; epidemics occurred only in lakes with steep-sided basins. In these lakes, the magnitude of epidemics varied with year. We suggest that biological (predation) and physical (turbulence) effects of basin shape interact with annual weather patterns to determine the regional distribution of this parasite.

Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity?

We studied the selection response of the freshwater grazing zooplankter, Daphnia galeata, to increased abundance of cyanobacteria in its environment. Cyanobacteria are a poor-quality and often toxic food. Distinct genotypes of D. galeata were hatched from diapausing eggs extracted from three time horizons in the sediments of Lake Constance, Europe, covering the period 1962 to 1997, a time of change in both the prevalence of planktonic cyanobacteria and levels of phosphorus pollution. We assessed whether the grazers evolved to become more resistant to dietary cyanobacteria by exposing genetically distinct clones to two diets, one composed only of the nutritious green alga, Scenedesmus obliquus (good food), and the other a mixture of S. obliquus and the toxic cyanobacterium Microcvstis aeruginosa (poor food). Genotype performance was measured as the specific rate of weight gain from neonate to maturity (gj). We evaluated evolutionary change in the Daphnia population using an analysis of reaction norms based on relative (log-transformed) changes in gj. Log(gj) is a measure of the proportional effect of dietary cyanobacteria on other fitness components of the Daphnia phenotype. For comparison, we also analyze absolute (i.e., nontransformed) changes in gj and discuss the interpretations of the two approaches. Statistical results using a general linear model demonstrate a significant effect of genotype (showing differences in gj among genotypes), a significant genotype x food-type interaction (showing differences in phenotypic plasticity among genotypes), and, in the case of log-transformed data, a significant sediment-genotype-age x food-type interaction. The latter shows that phenotypic plasticity evolved over the period studied. Two constraints act on response to selection in the D. galeata-Lake Constance system. First, gj on a diet containing poor food is highly correlated with gj on a diet of good food, thus evolving resistance also meant evolving an increase in gj on both diets. Second, because genotypes with a high gj also grow to a large adult body size, which in turn increases Daphnia vulnerability to fish predation, we suggest that selection only acted to favor genotypes possessing a high potential gj after cyanobacteria became prevalent. The presence of cyanobacteria depressed realized gj and led to animals of small adult body size even if their genotypes had the potential for high gj and large size. With realized gj reduced, genotypes with an inherently high value could be selected even in the presence of predatory fish. The joint action of selection by dietary cyanobacteria and vulnerability to fish predation provides an explanation for the observed evolution of resistance to poor food through reduced phenotypic plasticity.

Temporal variation, dormancy, and coexistence: a field test of the storage effect.

Theoretical models suggest that overlapping generations, in combination with a temporally fluctuating environment, may allow the persistence of competitors that otherwise would not coexist. Despite extensive theoretical development, this "storage effect" hypothesis has received little empirical attention. Herein I present the first explicit mathematical analysis of the contribution of the storage effect to the dynamics of competing natural populations. In Oneida Lake, NY, data collected over the past 30 years show a striking negative correlation between the water-column densities of two species of suspension-feeding zooplankton, Daphnia galeata mendotae and Daphnia pulicaria. I have demonstrated competition between these two species and have shown that both possess long-lived eggs that establish overlapping generations. Moreover, recruitment to this long-lived stage varies annually, so that both daphnids have years in which they are favored (for recruitment) relative to their competitor. When the long-term population growth rates are calculated both with and without the effects of a variable environment, I show that D. galeata mendotae clearly cannot persist without the environmental variation and prolonged dormancy (i.e., storage effect) whereas D. pulicaria persists through consistently high per capita recruitment to the long-lived stage.