Weakly interacting species as drivers of ecological stability

Abstract

Determining how individual species can act to moderate the stability of entire ecosystems is a pressing challenge in a world undergoing rapid environmental change. Here, we show that even very weakly interacting species with no discernible effect on ecological dynamics can contribute substantially to ecosystem stability. Further, the nature of this contribution depends on biotic context, and both the type and complexity of interspecific interactions in the community. By manipulating multitrophic aquatic microcosm communities experimentally, we found that the contributions of a bacteriophage parasite to overall system stability following a pulse perturbation were variously stabilizing, destabilizing and neutral, depending on the presence of competitor or predator species of its bacterial host. This was despite the phage itself having no detectable effect on the biomass or growth rates of its host. Our results demonstrate the pivotal importance of both weak and indirect interactions in moderating the stability of whole ecological networks, and have profound implications for our ability to predict the consequences of perturbations on ecosystems.

Keywords: community ecology; ecology; experiment; microcosm; species interactions; stability.

Figure 1.

Our microcosm food webs and experimental design. (a) Our experimental treatments consisted of communities comprising host bacteria Bacillus subtilis (in blue), in combination with either competitor bacterium Serratia marcescens (red), the predatory protist Paramecium caudatum (green) or both together. Specialist parasitic bacteriophage of B. subtilis, SPP1 phage, was added to half of microcosms in each community treatment and microcosms were assigned to perturbed or unperturbed treatments in a factorial design, with each of our 12 experimental treatments replicated seven times. (b) We quantified the contribution of SPP1 phage to the resistance, reactivity, resilience and temporal variability of communities (see table 1 for a detailed description of stability components and their quantification) by comparing stability responses in communities in which the phage was present (purple lines) and those in which it was not (yellow lines) through comparison of perturbed (bold lines) with equivalent unperturbed (faded lines) treatments. If a measure of stability was increased in the absence of the phage compared with when it was present, this implies that the phage contributes negatively to this measure of stability, and vice versa.

Figure 2.

Normalized (mean standardized; overall mean across treatments represented by dashed line) densities (mean ± s.e.m., n = 7) of each of Bacillus subtilis (host species), Serratia marcescens (competitor), Klebsiella, Paramecium caudatum (predator) and our focal SPP1 phage in our experimental treatments in which S. marcescens was present (a–d,i,j), P. caudatum was present (e–j), and all species were present (k,l) in both unperturbed (left column) and perturbed (right column) communities. Shown are the combined data from experimental days 5−10, following the perturbation on experimental day 4. Data for individual populations over time are shown in electronic supplementary material, figures S1–S3.

Figure 3.

Phage contributions to multiple components of ecological stability (mean log response ratio (LRR) ± 95% CI; see table 1 for a description of stability components and their quantification and interpretation; the metrics here were log (x + a)-transformed, where a was a constant such that when added the minimal value was 1) in microcosm communities containing competition with Serratia marcescens (red dots) or predation by Paramecium caudatum (green dots) and in complex communities containing both competition and predation (blue dots).

Figure 4.

Competitive ability of Bacillus subtilis isolates, measured as the ratio of B. subtilis to Serratia marcescens (dashed line indicates a 1 : 1 ratio, solid line represents ancestral competitive ability) in both the presence and absence of the bacteriophage parasite in (a) unperturbed and (b) perturbed communities.