Complex Trophic Interactions in an Acidophilic Microbial Community

Abstract

Extreme habitats often harbor specific communities that differ substantially from non-extreme habitats. In many cases, these communities are characterized by archaea, bacteria and protists, whereas the number of species of metazoa and higher plants is relatively low. In extremely acidic habitats, mostly prokaryotes and protists thrive, and only very few metazoa thrive, for example, rotifers. Since many studies have investigated the physiology and ecology of individual species, there is still a gap in research on direct, trophic interactions among extremophiles. To fill this gap, we experimentally studied the trophic interactions between a predatory protist (Actinophrys sol, Heliozoa) and its prey, the rotifers Elosa woralli and Cephalodella sp., the ciliate Urosomoida sp. and the mixotrophic protist Chlamydomonas acidophila (a green phytoflagellate, Chlorophyta). We found substantial predation pressure on all animal prey. High densities of Chlamydomonas acidophila reduced the predation impact on the rotifers by interfering with the feeding behaviour of A. sol. These trophic relations represent a natural case of intraguild predation, with Chlamydomonas acidophila being the common prey and the rotifers/ciliate and A. sol being the intraguild prey and predator, respectively. We further studied this intraguild predation along a resource gradient using Cephalodella sp. as the intraguild prey. The interactions among the three species led to an increase in relative rotifer abundance with increasing resource (Chlamydomonas) densities. By applying a series of laboratory experiments, we revealed the complexity of trophic interactions within a natural extremophilic community.

Keywords: Rotifera; acid mine drainage; extremophiles; food web; heliozoa; intraguild predation; mining lakes.

Figure 1

Feeding of Actinophrys sol on rotifers and ciliates after 24 h. Proportion of A. sol having eaten (a) a Cephalodella sp. individual or (b) an Elosa woralli individual. (c) Difference in ciliate numbers without and with A. sol per well. W-f, well-fed; St, staved; + Chl, 100,000 cells mL⁻¹, Chlamydomonas added. Mean ± standard error, n = 3 sets of 24–30 individual wells. For rotifers, both the treatment and the species effect were significant, p < 0.001, as was the species x treatment interaction (p < 0.001). For ciliates, no treatment effect was found (p = 0.07).

Figure 2

Time course of Heliozoan prey (a, Cephalodella sp.; b Elosa woralli; c, Urosomoida sp.) with and without A. sol. Mean ± standard error (n = 3). Abundance of both rotiferan prey differed between treatments (p = 0.03 for both) and also for ciliates (p << 0.001). Note different y-axis scales.

Figure 3

Relative contribution of Cephalodella sp. to total consumer abundance at varying productivity levels. Data were combined from the micro-scale experiments (Micro-Expts) mean ± standard error, the meso-scale experiments (Meso-Expts) and field data for mean abundances over a three-year observation period (field data from [25]). Solid line, trend curve fit.

Figure 4

Schematic representation of the relationship of resource availability and consumer and predator abundance.