Eutrophication governs predator-prey interactions and temperature effects in Aedes aegypti populations

Abstract

Background: Mosquito population dynamics are driven by large-scale (e.g. climatological) and small-scale (e.g. ecological) factors. While these factors are known to independently influence mosquito populations, it remains uncertain how drivers that simultaneously operate under natural conditions interact to influence mosquito populations. We, therefore, developed a well-controlled outdoor experiment to assess the interactive effects of two ecological drivers, predation and nutrient availability, on mosquito life history traits under multiple temperature regimes.

Methods: We conducted a temperature-controlled mesocosm experiment in Kruger National Park, South Africa, with the yellow fever mosquito, Aedes aegypti. We investigated how larval survival, emergence and development rates were impacted by the presence of a locally-common invertebrate predator (backswimmers Anisops varia Fieber (Notonectidae: Hemiptera), nutrient availability (oligotrophic vs eutrophic, reflecting field conditions), water temperature, and interactions between each driver.

Results: We observed that the effects of predation and temperature both depended on eutrophication. Predation caused lower adult emergence in oligotrophic conditions but higher emergence under eutrophic conditions. Higher temperatures caused faster larval development rates in eutrophic but not oligotrophic conditions.

Conclusions: Our study shows that ecological bottom-up and top-down drivers strongly and interactively govern mosquito life history traits for Ae. aegypti populations. Specifically, we show that eutrophication can inversely affect predator-prey interactions and mediate the effect of temperature on mosquito survival and development rates. Hence, our results suggest that nutrient pollution can overrule biological constraints on natural mosquito populations and highlights the importance of studying multiple factors.

Keywords: Anthropogenic pressures; Biodiversity decline; Ecological drivers; Interaction effects; Temperature; Vector-borne.

Fig. 1

Setup of the mesocosm experiment in Skukuza, Kruger National Park. a Schematic drawing of a mesocosm, courtesy of Erik-Jan Bosch. b Mean temperatures in each of the temperature treatments ± standard error (SE), as measured with i-buttons in the different mesocosms during the entire period of the mesocosm experiment. Except for the lowest temperature treatment, all treatments contained aquarium heaters. c Overview of the setup. d Locations in and around Kruger National Park (indicated with red dots) where concentrations of inorganic phosphorus were measured to determine the median eutrophication status for the experiment

Fig. 2

Overview of eutrophication variables (a, b) (NO₃, PO₄) and abiotic variables (c, d): pH; tds, total dissolved salts; EC (mV), electro conductivity in mS per cm. All data shown as the mean ± standard error (SE). Treatments with and without predators were merged in this table. Different letters indicate significant differences between treatments at α = 0.05

Fig. 3

Effect of eutrophication and predation as interacting pressures on emergence of adult Ae. aegypti. Bars indicate average cumulative emergence across all temperature regimes ± standard error (SE). Although there was a significant effect of temperature influencing the number of adults emerged, there were no significant interactions between temperature and eutrophication/predation, such that the pattern shown in the figure is representative across temperature treatments. Fractions are shown for illustration purposes only; statistics were done on the cumulative number of emerged adults. Star indicates a significant difference at α = 0.05

Fig. 4

Effect of eutrophication and predation treatments on the odds of emergence of females (a), emergence of males (b) and larval survival (c). Statistics shown above each of the panels depict results from a logistic regression model. Each symbol represents the average across all temperature regimes. NS indicates P > 0.05

Fig. 5

Effect of eutrophication, temperature and predation on development rate of Aedes aegypti. a Results for eutrophic conditions. b Results for oligotrophic conditions. Fits in a are for illustrative purposes only