Phosphorus limitation enhances parasite impact: feedback effects at the population level

Abstract

Background: Nutrient deficiency affects the growth and population dynamics of consumers. Endoparasites can be seen as consumers that drain carbon (C) or energy from their host while simultaneously competing for limiting resources such as phosphorus (P). Depending on the relative demands of the host and the parasite for the limiting nutrient, intensified resource competition under nutrient limitation can either reduce the parasite’s effect on the host or further reduce the fitness of the nutrient-limited host. So far, knowledge of how nutrient limitation affects parasite performance at the host population level and how this affects the host populations is limited. Results: We followed the population growth of Daphnia magna that were uninfected or experimentally infected with a microsporidian, Glugoides intestinalis. The Daphnia were fed either P-sufficient or P-limited algae. The P-limited diet decreased the population density and biomass compared with the populations fed with the P-sufficient algae. In the P-sufficient populations, infection with the parasite reduced the population density but not the biomass of Daphnia, while in the P-limited populations, both the density and biomass of Daphnia decreased toward the end of the 32 day experiment compared with the uninfected controls. The infected animals from the P-limited populations had higher parasite spore cluster counts, while, in a separate experiment, host diet quality did not affect the number of parasites in individually kept Daphnia. Conclusions: Because host diet quality did not affect parasite numbers at the individual level, we suggest that the higher parasite load in the P-limited populations is a result of feedback effects arising at the population level. Because of the density-dependent transmission of the parasite and the time lag between exposure and transmission, the lower host population density in the P-limited populations led to a higher spore:host ratio. This effect may have been further reinforced by decreases in filtration rates caused by crowding in the P-sufficient populations and/or increases in filtration rates as a response to poor food quality in the P-limited populations. The increases in exposure led to a higher parasite load and aggravated the negative effects of parasite infection at the population level.