Larval superiority of Culex pipiens to Aedes albopictus in a replacement series experiment: prospects for coexistence in Germany

Abstract

Background: The Asian tiger mosquito Aedes albopictus is an extremely invasive, globally distributed and medically important vector of various human and veterinary pathogens. In Germany, where this species was recently introduced, its establishment may become modulated by interspecific competition from autochthonous mosquito species, especially Culex pipiens (s.l.). While competitive superiority of Ae. albopictus to Cx. pipiens (s.l.) has been described elsewhere, it has not been assessed in the epidemiological conditions of Germany. The present study aimed to determine if such superiority exists under the physicochemical and microclimatic conditions typical for container habitats in Germany.

Methods: In a replacement series experiment, the larval and pupal responses of Ae. albopictus and Cx. pipiens (s.l.) (mortality, development time, growth) to interspecific interaction (five larval ratios) at (sub-)optimal temperatures (15, 20 and 25 °C) and differing food supply (3 and 6 mg animal-based food larva^-1) were investigated using a randomized split-plot design. In addition to physicochemical measurements of the test media, natural physicochemical conditions were determined for comparative analyses in mosquito breeding sites across the Rhine-Main metropolitan region of Germany.

Results: Under the physicochemical and microclimatic conditions similar to the breeding sites of the Rhine-Main region, competitive superiority of Cx. pipiens (s.l.) to Ae. albopictus in terms of larval survival was more frequently observed than balanced coexistence. Food regime and multifactorial interactions, but not temperature alone, were controlling factors for interspecific competition. Larval food regime and the larval ratio of Ae. albopictus influenced the physicochemistry and algal growth at 15 °C, with increased Ae. albopictus mortality linked to a decreasing number of Scenedesmus, Oocystis and Anabaena algae.

Conclusions: Under the present environmental conditions, the spread of Ae. albopictus from isolated foci in Germany may generally be slowed by biotic interactions with the ubiquitous Cx. pipiens (s.l.) (and potentially other container-breeding mosquito species) and by limnic microalgae in microhabitats with high resource levels. Detailed knowledge of the context dependency in temperate mosquito ecology, and interrelations of physicochemistry and phycology may help to achieve a better understanding of the upcoming Ae. albopictus colonization processes in central and northern Europe.

Keywords: Interspecific competition; Microalgae; Niche differentiation; Resource competition; Water chemistry.

Fig. 1

Physicochemistry in established and potential larval mosquito microhabitats. a Physicochemistry in natural habitats of Cx. pipiens in the periphery of Frankfurt am Main, Germany, during September and October 2010. Temperature (°C), pH, conductivity (μS cm^-1) and dissolved oxygen concentration (mg l^-1) (mean ± SD) and respective Cx. pipiens abundance [# larvae: number of larvae (n = number of microhabitats)] are shown. Grey bars denote overall 95% confidence intervals. Key: 1, car tires; 2, vases; 3, rain barrels; 4, small reservoirs (bucket, plastic tarpaulin, pot, steel girder); 5, large reservoirs (metal and plastic tub, excavator shovel, water bowl); 6, dung discharge; 7, puddles; 8, ponds. b Spline curve of daily water temperature [mean ± SD] in 1 litre plastic cups logged from mid-May to end of July 2011. The cups representing potential mosquito habitats had been set up in shaded versus sunny localities in Frankfurt am Main

Fig. 2

Larval mortality [mean, SD] of Aedes albopictus and Culex pipiens in pure and mixed cohorts (x-axis - the number of Ae. albopictus: Cx. pipiens larvae) in dependence of temperature and larval food regime. Squares symbolize artificially set zero values; solid lines and broken lines - non-linear regression (second-order model); dotted lines - 95% confidence interval

Fig. 3

Mean pupation time PT₅₀ (days; box-plot with Tukey whiskers, mean shown as ‘+’) of Aedes albopictus and Culex pipiens in dependence of gender, the larval ratio (number of Ae. albopictus: Cx. pipiens larvae - Ae: Cx), temperature and larval food regime

Fig. 4

Daily accumulation of biomass (BA, mean ± SD) of individual female Aedes albopictus and Culex pipiens during their aquatic part of life in dependence of larval ratio, temperature and larval food regime. Solid line - linear regression; dotted lines - 95% confidence interval

Fig. 5

Algal growth in test vessels at 15 °C. Algal cells (mean and SD) grown in test media with pure and mixed cohorts of Aedes albopictus and Culex pipiens larvae in dependence of larval ratio (Ae:Cx - number of Ae. albopictus: Cx. pipiens larvae) and larval food regime with (a) 3 mg larva^-1 larval food supply versus (b) 6 mg larva^-1 larval food supply at 15 °C. Algal growth was not observed in test vessels at 20 °C and 25 °C