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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.

SUBMITTER: Pulkkinen K

PROVIDER: S-EPMC4223164 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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

Pulkkinen Katja K Wojewodzic Marcin W MW Hessen Dag O DO

BMC ecology 20141031

<h4>Background</h4>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 n ...[more]

PMID: 25366521

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Project description:Assessing algal nutrient limitation is critical for understanding the interaction of primary production and nutrient cycling in streams, and nutrient diffusing substrate (NDS) experiments are often used to determine limiting nutrients such as nitrogen (N) and phosphorus (P). Unexpectedly, many experiments have also shown decreased algal biomass on NDS P treatments compared to controls. To address whether inhibition of algal growth results from direct P toxicity, NDS preparation artifacts, or environmental covariates, we first quantified the frequency of nutrient inhibition in published experiments. We also conducted a meta-analysis to determine whether heterotrophic microbial competition or selective grazing could explain decreases in algal biomass with P additions. We then deployed field experiments to determine whether P-inhibition of algal growth could be explained by P toxicity, differences in phosphate cation (K vs. Na), differences in phosphate form (monobasic vs. dibasic), or production of H2O2 during NDS preparation. We found significant inhibition of algal growth in 12.9% of published NDS P experiments as compared to 4.7% and 3.6% of N and NP experiments. The meta-analysis linear models did not show enhanced heterotrophy on NDS P treatments or selective grazing of P-rich algae. Our field experiments did not show inhibition of autotrophic growth with P additions, but we found significantly lower gross primary productivity (GPP) and biomass-specific GPP of benthic algae on monobasic phosphate salts as compared to dibasic phosphate salts, likely because of reduced pH levels. Additionally, we note that past field experiments and meta-analyses support the plausibility of direct P toxicity or phosphate form (monobasic vs. dibasic) leading to inhibition of algal growth, particularly when other resources such as N or light are limiting. Given that multiple mechanisms may be acting simultaneously, we recommend practical, cost-effective steps to minimize the potential for P- inhibition of algal growth as an artifact of NDS experimental design.

Dataset Information

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

Publications

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

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