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.
The relationship between energy reserves (biomass and triacylglycerol) and starvation time is investigated for two planktonic Cladocera, Daphnia. galeata mendotae and Daphnia magna. Triacylglycerol storage is correlated to total individual biomass independently of body size. Adult biomass increases twofold to threefold during the intermolt, with triacylglycerol accounting for 16% of the total increase. The amount of triacylglycerol transferred into each egg depends on the adult’s feeding success. Starvation time is correlated to body mass; however, triacylglycerol storage and reproductive allocation modify the relationship. Although adult biomass and percentage of lipid both increase during intermolt, animals in late intermolt starve sooner than those in early‐middle intermolt because of the transfer of energy reserves to the ovaries for reproduction. Daphnia magna neonates with high maternal lipid survived twice as long as neonates with low maternal lipid but similar body mass.
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).
Epidemiologists increasingly realize that species interactions (e.g. selective predation) can determine when epidemics start and end. We hypothesize here that resource quality can also strongly influence disease dynamics: epidemics can be inhibited when resource quality for hosts is too poor and too good. In three lakes, resource quality for the zooplankton host (Daphnia dentifera) was poor when fungal epidemics (Metschnikowia bicuspidata) commenced and increased as epidemics waned. Experiments using variation in algal food showed that resource quality had conflicting effects on underlying epidemiology: high-quality food induced large production of infective propagules (spores) and high birth rate but also reduced transmission. A model then illustrated how these underlying correlations can inhibit the start of epidemics (when spore production/birth rate are too low) but also catalyse their end (when transmission becomes too low). This resource quality mechanism is likely to interface with other ones controlling disease dynamics and warrants closer evaluation.
Lake size and depth mediate the strength of interaction between fish and zooplankton. We test whether this variation in zooplanktivory indirectly affects the phytoplankton by comparing 19 lakes that represent two food webs resulting from the absence of piscivores in small, partial-winterkill lakes. Lakes with piscivorous fish are further distinguished by thermal stratification, which provides a refuge for zooplankton to avoid fish predation. We contrasted phytoplankton abundance in these three categories of lakes over six years, using both direct measures of concentration and a growth bioassay that measures phytoplankton from the perspective of a standard grazer (Daphnia). Contrary to expectations, phytoplankton abundance was largely unaffected by trophic structure or the presence of a deep-water refuge. However, grazer growth differed dramatically among the three categories of lakes. Consistent with trophic cascade, increased fish planktivory resulted in more phytoplankton food as measured from the grazer's perspective. This effect was independent of lake productivity or total abundance and size of phytoplankton. Instead, variation in food quality for grazers was associated with compositional differences in phytoplankton. These results indicate that persistent trophic cascades are more dramatic in the plankton than previously realized but primarily influence composition, rather than biomass. Although cryptic, such top-down effects create functional variation in grazer-resource coupling.
Parasites steal resources that a host would otherwise direct toward its own growth and reproduction. We use this fundamental notion to explain resource-dependent virulence in a fungal parasite (Metschnikowia)-zooplankton host (Daphnia) system and in a variety of other disease systems with invertebrate hosts. In an experiment, well-fed hosts died faster and produced more parasites than did austerely fed ones. This resource-dependent variation in virulence and other experimental results (involving growth and reproduction rate/timing of hosts) readily emerged from a model based on dynamic energy budgets. This model follows energy flow through the host, from ingestion of food, to internal energy storage, to allocation toward growth and reproduction or to a parasite that consumes these reserves. Acting as a consumer, the parasite catalyzes its own extinction, persistence with an energetically compromised host, or death of the host. In this last case, more resources for the host inadvertently fuels faster parasite growth, thereby accelerating the demise of the host (although the opposite result arises with different resource kinetics of the parasite). Thus, this model can explain how resource supply drives variation in virulence. This ecological dependence of virulence likely rivals and/or interacts with genetic mechanisms that often garner more attention in the literature on disease.
The genus Daphnia (Crustacea: Branchipoda) includes a diversity of species that are generalist grazers on plankton in freshwater lakes. Despite substantial intraspecific variation in body size, explanations of functional differences among Daphnia species continue to emphasize body size. In this study, we ask whether Daphnia in a relatively narrow range of body sizes differ in ability to exploit the array of resources commonly encountered in lakes. We compared juvenile growth rates of several clones and species of Daphnia fed natural planktonic resources that differed in overall dietary richness. We observed, both among and within species, a trade-off between growth rates in rich and poor resource conditions. We compared the ability of different species and clones to exploit natural resources in a lake mesocosm experiment, testing the prediction that clones displaying the greatest growth rates in rich resource conditions would have the highest minimum resource requirements.Using 8000-L whole water column enclosures, replicate populations of D. rosea and two different morphs of D. pulicaria were established separately in monoculture in a thermally stratified lake. An additional treatment without crustacean zooplankton was also established. We quantified resources in the enclosures using multiple indirect measures (e.g., chlorophyll a) and a growth bioassay. Results supported predictions; rankings of resource levels achieved in the different treatments suggest that Daphnia trade off high maximum growth rates for low minimum resource requirements. This field experiment also documented large differences among the species and clones of Daphnia in their impact on phytoplankton resources, water clarity, and formation of calcite particles (whiting). We suggest that these large ecological effects stem from the trade-off in abilities to use rich vs. poor resources and constitute an important aspect of grazer-resource interactions.We review the literature on growth and reproductive responses of zooplankton species to resource level and find general agreement with the concept of a trade-off between abilities to exploit rich and poor resource conditions. A reanalysis of data from a comprehensive study on Daphniidae growth confirms our results and suggests that the breadth of species in this family conforms to the trade-off. Furthermore, the trade-off is only weakly, and not significantly, associated with body size. Our study presents a new framework for understanding the functional significance of daphniid diversity to plankton food webs and illustrates how an ecological trade-off provides a means of linking species diversity to ecosystem function.
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